REVIEW

Microalgae: An Exciting Alternative Protein Source and Nutraceutical for the Poultry Sector

LiXue Zhang1https://orcid.org/0009-0001-3144-0864, YuNan Jiang2https://orcid.org/0009-0002-7999-0029, Jameel Ahmed Buzdar3https://orcid.org/0009-0005-7141-4555, Shabbir Ahmed4https://orcid.org/0009-0000-3240-7479, XinYu Sun2https://orcid.org/0009-0000-6677-5050, FengHui Li2https://orcid.org/0009-0007-4253-4093, LiNa Ma2https://orcid.org/0009-0007-3241-6974, Pei Feng Wu2https://orcid.org/0009-0002-9604-3672, ChangXing Li2,*https://orcid.org/0009-0002-5062-4826
Author Information & Copyright
1School of Medicine, Northwest Minzu University, Lanzhou 730030, China
2Department of Human Anatomy, Medical College of Qinghai University, Xining 810016, China
3Faculty of Veterinary and Animal Sciences, Lasbela University of Agriculture, Water and Marine Sciences, Uthal 3800, Pakistan
4Faculty of Animal Husbandry & Veterinary Science, Sindh Agriculture University Tandojam, Tandojam 70050, Pakistan
*Corresponding author : ChangXing Li, Department of Human Anatomy, Medical College of Qinghai University, Xining 810016, China, Tel: +86-0971-6143168, Fax: +86-0971-6143168, E-mail: lichangxing@qhu.edu.cn

© Korean Society for Food Science of Animal Resources. This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: Oct 16, 2024 ; Revised: Nov 21, 2024 ; Accepted: Dec 02, 2024

Published Online: Jan 01, 2025

Abstract

Microalgae have garnered a considerable attention as a sustainable substitute as customary feed ingredients for poultry, predominantly due to their extraordinary nutritive profile and purposeful properties. These minuscule organisms are protein rich, retain an ample quantity of essential fatty acids, vitamins, minerals, and antioxidants, thus are capable of improving nutritive value of poultry diets. Microalgae comparatively delivers an outstanding source of protein containing substantial amount of innumerable bioactive complexes, omega-3 fatty acids in addition to the essential amino acids (methionine and lysine), crucial for optimal growth and development. Besides nutritional significance, microalgae have considerable immunomodulatory and antioxidant properties that help to reduce oxidative stress and enhance immune status, thereby improving the overall health and performance. Additionally, microalgae proved to induce antimicrobial and intestinal health benefits via upregulated gut eubiosis, promoting the colonization and growth of probiotic bacteria and offering protection against infections. These nutraceutical benefits are particularly important for sustainable poultry production and reducing the dependence on antibiotic growth promoters to produce antibiotic free food. This review aims to highlights multifaceted advantages of microalgae as a functional feed additive for poultry diet to support sustainable and efficient poultry production.

Keywords: microalgae; nutraceutical potential; alternative protein source; health benefits; poultry

Introduction

Poultry farming is vital to the worldwide livestock sector, providing a substantial source of protein and nutrition for growing humans population (Mottet and Tempio, 2017). The demand for poultry products has been gradually increasing due to numerous factors including population increase, rising income levels, and evolving dietary preferences (Clonan et al., 2016; Saeed et al., 2019; Yatao et al., 2018). The poultry industry constitutes a significant segment of the global agricultural sector, especially in developing nations (Mnisi et al., 2023), where ever rising human population needs the introduction of alternative sources of dietary protein to avoid the hazards related to protein deficits (Mnisi et al., 2023). Poultry plays a crucial role in global food security by providing affordable, high-quality protein in the form of meat and eggs. Poultry is a vital source of meat and eggs containing high-quality proteins, enriched with essential amino acids, vitamins and minerals to fulfill the nutritional requirements, vital for addressing malnutrition and combat food security issues in low-income population (Gržinić et al., 2023; Lingala et al., 2024). Additionally, the contribution of poultry in food security extends beyond the nutritional requirements. It plays an important role to enhance the livelihood of low-income population, owing to the economically viable and short production life (Vlaicu et al., 2024). Nonetheless, the manufacturing of poultry products demonstrates several obstacles, including environmental degradation, elevated feed costs, and the dissemination of diseases (Mottet and Tempio, 2017). Another hurdle which increase of feed price is the extravagant feed ingredients, including grains, oilseeds, synthetic chemicals and feed supplements to raise the production cost (Arif et al., 2017; Safdar et al., 2024). To tackle these difficulties, there is increasing interest in identifying alternative feed ingredients that can improve the nutritional quality of poultry diets simultaneously reducing the adverse environmental effects of poultry production (Arain et al., 2022b; Nabi et al., 2020a; Nabi et al., 2020b; Saeed et al., 2018). Poultry feed researchers emphasize for the investigation of alternative feed ingredients, including novel protein sources, insect-derived feed, algae, and plant-based bioactive substances from the food and agricultural sectors, to substitute expensive ingredients and attain production objectives (Behan et al., 2024; Nabi et al., 2024).

Microalgae are photosynthetic microorganisms acknowledged as a viable alternative feed component in poultry diets owing to their elevated nutritional content and functional attributes (Koyande et al., 2019). Furthermore, microalgae represent a wide assemblage of organisms capable of thriving in various settings, including freshwater (Maltsev and Maltseva, 2021), marine water (Bhuvana et al., 2019), and waste water. They are an abundant source of protein and vital fatty acids (Sathasivam et al., 2019), vitamins (Wang et al., 2021), minerals (Uribe-Wandurraga et al., 2019), and source of antioxidants (Gauthier et al., 2020), all these constitute essential elements of a balanced poultry diet (Madeira et al., 2017). While, microalgae have demonstrated the ability to augment the growth and immune response of poultry, in addition to enhancing the quality of poultry products (El-Ghany, 2020). These microscopic photosynthetic organisms are a sustainable and renewable resource, containing higher concentration of essential nutrients, supporting the growth and productive performance of poultry. The lipid fraction, of microalgae particularly omega-3 fatty acids like docosahexaenoic acid (DHA), boost immunity and promoting gut health, thus enhances the productivity and nutritional quality of poultry based food such as meat and eggs (Kalia and Lei, 2022).

Present study provides a comprehensive overview of the current understanding on incorporation of microalgae in poultry diets. Moreover, current review offers a comprehensive analysis of the nutritional value, functional features, and advantageous applications of microalgae in poultry nutrition to improve the health and productivity of poultry. Simultaneously, the prospective advantages and obstacles related to the use of microalgae in poultry feed should also be emphasized.

Categories and Characteristics of Microalgae

Microalgae constitute a complex assemblage of photosynthetic microorganisms inhabiting a variety of aquatic habitats, encompassing both freshwater and marine ecosystems (Saber et al., 2022). They are essential to global ecological and biogeochemical cycles, greatly contributing to primary production and serving as the foundation of the food sources for aquatic animals (Lobus and Kulikovskiy, 2023; Quintas-Nunes et al., 2023). These unicellular or multicellular microbes may utilize both organic and inorganic carbon sources for growth and development, rendering them an optimal platform for large-scale biomass production (Chen et al., 2024). The diversity of microalgae exemplifies their flexibility and the extensive variety ranging from unicellular species like Chlorella to multicellular forms like Spirogyra. Their ability to adapt to diverse habitats, including extreme environmental settings (Singh et al., 2023).

The classification of microalgae is intricate owing to their extensive diversity and the ongoing identification of novel species. They are often categorized according to their pigmentation, cell wall composition, storage products, and various morphological and physiological characteristics (Shaikh et al., 2022). Microalgae are taxonomically categorized into numerous principal groups, including green algae, diatoms, cyanobacteria, and dinoflagellates, among others (de Morais et al., 2016; Masojídek and Torzillo, 2014). The distinct attributes of each category, including their pigment makeup, cellular architecture, and metabolic pathways, influence their distinctive qualities and prospective applications (Madkour et al., 2023; Masojídek and Torzillo, 2014).

Green algae are recognized for their capacity to a mass substantial lipid levels, rendering them a prospective source for biofuel production (Dolganyuk et al., 2020; Khan et al., 2018). Diatoms are acknowledged for their capabilities in wastewater treatment and the synthesis of key biochemical, such as carotenoids and silica (Quintas-Nunes et al., 2023). Cyanobacteria, sometimes referred as blue-green algae, have attained interest for their capacity to synthesize a diverse array of bioactive substances, such as pigments, vitamins, and antioxidants.

Nutritional Composition of Microalgae

Microalgae possess the capability to synthesize a diverse array of important substances, such as proteins, lipids, carbohydrates, vitamins, and pigments, which are utilized in the feed, medicinal, and biofuel sectors (Dolganyuk et al., 2020). The scientific investigation of microalgae has attracted heightened interest in recent years owing to its exceptional potential as a sustainable and nutrient-rich source of feed, and valuable bioactive chemicals (Bature et al., 2022).

The nutritional makeup of microalgae can vary considerably based on species, growth conditions, and post-harvest processing techniques (Alghazeer et al., 2022). Light intensity, temperature, nutrient availability, and growth strategies can all affect the accumulation of certain nutrients in microalgae cells. The fundamental advantage of microalgae is their remarkable nutritional profile. Microalgae are recognized for their abundance of vital elements, such as proteins, carbs, lipids, vitamins, and minerals (Sanjari et al., 2018). The energy content of microalgae biomass is determined by the existence of carbon, oxygen, hydrogen, nitrogen, and other components, rendering them a viable source of renewable energy. Moreover, microalgae have evolved intricate biochemical and physiological mechanisms to thrive in extremely competitive environments, resulting in the accumulation of important bioactive chemicals (Rendón-Castrillón et al., 2020). Microalgae can possess a remarkable protein concentration, with certain species up to 70% protein on a dry matter basis (Sanjari et al., 2018). These proteins are often of superior quality, encompassing all essential amino acids necessary to meet the nutritional requirements of animals. Moreover, microalgae serve as a substantial source of omega-3 and omega-6 fatty acids, essential for augmenting immune response and improving the health and productivity of animals. Specific microalgae species are recognized as superior producers of carotenoids, including astaxanthin and lutein, which have strong antioxidant capabilities and are associated with numerous health advantages (Novoveská et al., 2023).

Moreover, microalgae are recognized as a substantial source of lipids, especially triacylglycerol’s, which can be utilized for many industrial purposes (de Morais et al., 2016). The lipid content of microalgae is affected by several parameters, including species, growing circumstances, and nutrient availability (Rendón-Castrillón et al., 2020). Besides lipids, microalgae also store considerable quantities of carbohydrates, which can improve their nutritional utility in cattle feed (de Morais et al., 2016). Furthermore, microalgae are distinguished by their pigments, including carotenoids and phycobilipigments, which enhance their vivid coloration and exhibit antioxidant and therapeutic attributes. Moreover, microalgae serve as a superior supplier of important vitamins and minerals, encompassing vitamin A, B-complex vitamins, vitamin C, vitamin E, along with minerals such as iron, calcium, and magnesium. Likewise, Dineshkumar et al. (2017) documented the biochemical and elemental analysis of green algae composition was depicted in Table 1. The nutritional value of microalgae can be augmented by crop optimization and genetic engineering.

Table 1. Chemical composition of various species of microalgae
Species of microalgae Carbohydrates Protein Lipids Total dietary fiber References
Chlorella vulgaris 20.99 15.67 41.51 15 Alfaia et al. (2021); Chia et al. (2015)
Spirulina platensis 30.21 13.3 48.36 14.98 Seghiri et al. (2019)
Chlorella sorokiniana 35.67 9.9 18.81 13.5 Chia et al. (2015); Niccolai et al. (2019)
Nannochloropsis oceanica 22.7 24.8 19.1 20 Zanella and Vianello (2020)
Scenedesmus obliquus 13.41 4.66 30.38 19.37 Ferreira et al. (2020)
Dunaliella tertiolecta 21.69 2.87 61.32 9.06 Araj‐Shirvani et al. (2024)
Dunaliella salina 32 57 9 48.82 Shantkriti et al. (2023)
Scenedesmus dimorphus 36.5 13 28 32.7 Tapia-López et al. (2024)
Chlorococum humicola 32.5 - - 24.5 Yang et al. (2022)
Chlamydomonas reinhardtii 22.6 64.7 12.6 11.9 Darwish et al. (2020)
Spirogyra sp. 48.5 13 16 37 Sriwattana et al. (2024)
Porphyridium cruentum 48.5 33.5 11.5 21.7 Castro‐Varela et al. (2021)
D. salina 85.58 8.46 11.47 0.8 Demirel (2022)
Arthrospira platensis 42.08 14.95 6.5 42.82 Markou et al. (2023)
Scenedesmus almeriensis 49.4 24.6 1.58 22.6 Sánchez-Zurano et al. (2021)
Haematococcus pluvialis 32.59 0.13 3.24 34.56 Marinho et al. (2021)
C. vulgaris 45.64 59.71 19 21.16 Ricky et al. (2022)
Download Excel Table

Bioactive Constituents and Pharmaceutical Properties of Microalgae

Microalgae are acknowledged as a prolific and underutilized source of bioactive chemicals with significant potential for many uses. These microscopic photosynthetic organisms may manufacture a variety of primary and secondary metabolites, many of which possess valuable nutritional, medicinal, and industrial characteristics (Alghazeer et al., 2022). Typically, microalgae have been cultivated mainly for the synthesis of several recognized beneficial chemicals, including carotenoids, critical omega-3 fatty acids, and phycobilipigments (Quintas-Nunes et al., 2023). Recent study has revealed the significant untapped potential of microalgae, emphasizing the existence of several bioactive compounds with prospective nutraceutical and medicinal applications (Alghazeer et al., 2022; Mobin and Alam, 2017).

Microalgae have attracted interest for their capacity to generate a wide variety of bioactive secondary metabolites. These encompass substances possessing antioxidant, anti-inflammatory, antibacterial, and potential anti-cancer activities (Alghazeer et al., 2022; Mobin and Alam, 2017; Saha and Murray, 2018). The chemical composition and quantity of these bioactive molecules can fluctuate considerably based on factors such as species, growth circumstances, and environmental influences (Alghazeer et al., 2022; Quintas-Nunes et al., 2023). Bioactive molecules are typically secondary metabolites, encompassing a diverse array of chemicals such as organic acids, carbohydrates, amino acids, peptides, vitamins, growth regulators, antibiotics, enzymes, and poisonous compounds (de Morais et al., 2015; Munaro et al., 2021). The metabolites exhibit a diverse array of biological actions, encompassing anticancer, antiviral, antioxidant, and immunomodulatory properties (Arain et al., 2022a; Du et al., 2024). The possibility exists for the discovery of novel medication leads from these metabolites. Cyanobacteria are the most significant source of bioactive chemicals among numerous groups of microalgae (Martínez-Francés and Escudero-Oñate, 2018). In summary, the extensive diversity and unexploited potential of bioactive chemicals in microalgae signify a promising frontier in nutrition, medicines, and sustainable resource management.

Microalgae possess numerous pharmaceutical and nutraceutical properties, offering potential benefits for poultry health and performance. Research indicated that microalgae contains bioactive compounds such as carotenoids, omega-3 fatty acids, antioxidants, vitamins, and minerals, they are participated to enhance the immune responses and reduce oxidative stress in poultry (Abdelnour et al., 2019; Fig. 1). These bioactive compounds enhance the blood concentration of anti-oxidant enzyme like superoxide dismutase (SOD), glutathione peroxidase (GPx) and catalase (CAT), thereby reduced the oxidative stress by improving the antioxidant defense (Emam et al., 2024; Panaite et al., 2023). Furthermore, dietary supplementation of microalgae significantly reduces the oxidative stress by scavenging toxic radicals of reactive oxygen species (ROS) and also mitigated the negative effects of heat stress in broiler chicken (Chaudhary et al., 2023a). Another study, have revealed that mesobiliverdin IXα (MBV)-enriched microalgae extracts can improve gut health and microbial balance in broilers, increasing beneficial Lactobacillus species and promoting intestinal villi growth. Notably, MBV-SP2 lowered pro-inflammatory markers and improved intestinal morphology more effectively than antibiotic treatments, highlighting MBV-enriched extracts as a promising alternative for antibiotic-free broiler health management (Chang et al., 2021). Previously it was demonstrated broiler fed diet containing a mixture of Dunaliella salina and Spirulina (1.0 and 1.5 g/kg), significantly enhanced oxidative stress, body weight, feed efficiency, and immune response, in addition to boost the lipid profiles, liver and kidney function (Alghamdi et al., 2024). Additionally, microalgae possess antimicrobial and anti-inflammatory properties, helping to combat pathogens and reduce disease incidence (Pagels et al., 2022). As a natural and sustainable feed additive, microalgae present a promising strategy for boosting poultry health and productivity without relying on synthetic drugs (Fig. 1). Previously (Balakrishnan et al., 2021), suggested that fatty acid methyl esters derived from marine microalgae effectively inhibit Listeria monocytogenes growth, demonstrating potent antimicrobial properties by disrupting cellular metabolism and membrane integrity. Results also confirmed that fatty acid esters suppressed the biofilm formation and improved Caenorhabditis elegans survival in infection models, showing potential as a natural feed additive for poultry to control infection and Listeria contamination (Balakrishnan et al., 2021).

kosfa-45-1-243-g1
Fig. 1. Illustrates the potential positive impact of microalgae on poultry. ALT, alanine aminotransferase; ROS, reactive oxygen species; SOD, superoxide dismutase; GPX, glutathione peroxidase; PrxR, peroxiredoxin; H2O2, hydrogen peroxide.
Download Original Figure
Antioxidant activity

Prooxidants are typically xenobiotic or external compounds, such as certain chemicals, pollutants, and environmental toxins, they are responsible to promote the oxidative stress by increasing the production of free radicals of ROS and disrupted the body ability to neutralized these toxic agent (Rahal et al., 2014). Reactive molecules of oxygen derivatives produced during the process of ROS formation like superoxide anion (O2), hydrogen peroxide (H2O2) and hydrogen radicles (OH; Bergamini et al., 2004). The excessive production of these radicals interrupt the normal physiological function at cellular level, leading to cause serious damage and initiated the development of numerous pathological conditions including cancer, cardiovascular and neurodegenerative disorders (Arain et al., 2018).

Oxidative stress in poultry refers to the imbalance between the production of ROS and the bird’s ability to counteract these harmful molecules with antioxidants. Poultry birds are more susceptible to oxidative stress specially under intensive farming and heat stress conditions particularly in tropical and subtropical regions of the world. Several strategies have been implemented to reduce the oxidative stress such as adopting modern technologies, improved management, shifting of conventional forming practices into the environmental control farming practices and dietary manipulation (Saeed et al., 2017a). Several studies have been reported that nutritional intervention and use phytogenic feed additive (herbs and their derivative) are the effective strategy to reduce the incidence of heat stress and mitigate the negative effects of oxidative damage (Arain et al., 2024; Changxing et al., 2018; Hassan et al., 2023; Saeed et al., 2017b). Furthermore, it was demonstrated that antioxidants supplied through external dietary supplements, they play a crucial role in combating oxidative stress by scavenging ROS and boosting the activity of antioxidant enzyme in poultry birds (Aboamer et al., 2024; Ashraf et al., 2024).

Microalgae have recently attracted considerable interest for their exceptional potential as a source of vital bioactive chemicals, especially antioxidants. The bioactive substances found in microalgae, such as bioflavonoids, carotenoids, vitamins C and E, biometals, and omega-3 and 6 fatty acids, are particularly effective to regulate the oxidative stress and boost the anti-oxidant defense (Fernandes et al., 2020b; Kiran and Venkata Mohan, 2021). Microalgae naturally contains numerous antioxidant enzymes including SOD, CAT, GPx, and peroxiredoxin which play a crucial role in neutralizing the free radicals of ROS. These antioxidants either directly scavenge harmful radicals or regenerate other antioxidants, utilizing the reducing power generated through photosynthesis (Cirulis et al., 2013).

Multiple studies have documented the existence of a wide range of antioxidant chemicals in several microalgal species, such as Chlorella, Spirulina, and Dunaliella, among others (Coulombier et al., 2021). The antioxidant capabilities of microalgae stem from their capacity to neutralize free radicals, impede lipid peroxidation, and safeguard cells from damage generated by oxidative stress (Lucas et al., 2020; Saha and Murray, 2018; Sikiru et al., 2019).

Previous research has examined the antioxidant capabilities of Chlorella vulgaris, a green microalga recognized for its substantial nutritional benefits and medicinal attributes. C. vulgaris exhibits significant antioxidant activity, exceeding that of widely utilized synthetic antioxidants (Sikiru et al., 2019). The antioxidant characteristics of C. vulgaris are mainly attributed to the presence of abundant amount of carotenoids, vitamins, and several bioactive substances (Hamouda et al., 2022). Similarly, Spirulina, a blue-green microalga, has been thoroughly studied for its antioxidant characteristics, and recognized as a substantial source of phycocyanin, a powerful antioxidant pigment that demonstrates several therapeutic effects, including anti-inflammatory, neuroprotective, and anticancer properties (Alghazeer et al., 2022; Mamani et al., 2020; Sikiru et al., 2019). Similarly, Caulerpa filiformis, a green species of algae found in the Sechura Bay area of Peru, renowned for its powerful antioxidant potential, owing to the presence of numerous bioactive compounds (Laos et al., 2023). Besides their antioxidant characteristics, microalgae have been explored for possible applications in biofuel generation, wastewater treatment, and animal feed augmentation. The antioxidant capacity of microalgae is well-documented, and their utilization as a source of natural antioxidants presents a promising research avenue with considerable implications for enhancing the health and productivity of livestock animals (Mobin and Alam, 2017).

Anti-inflammatory activity

Inflammation is a key physiological process essential for the body’s defense against detrimental stimuli, like pathogens, damaged cells, or irritants (Rock et al., 2009). This intricate reaction encompasses a series of cellular and molecular activities aimed at eradicating the primary source of cellular harm, removing necrotic cells and tissues affected by the initial damage, and commencing the healing process.

The anti-inflammatory characteristics of microalgae derived from their diverse secondary metabolites, have demonstrated the ability to regulate immune system and reduced inflammatory reactions (Tolba et al., 2020). Microalgal species such as C. filiformis exhibit significant antioxidant and anti-inflammatory properties, perhaps attributable to their elevated levels of polyphenolic chemical (Pagels et al., 2022). Glycoglycerolipids, a category of glycolipids sourced from microalgae, have emerged as potential anti-inflammatory medicines. These compounds have been shown to possess several biological actions, including anti-inflammatory, antiviral, anticancer, and antibacterial properties, rendering them promising candidates for therapeutic development (Conde et al., 2021). Furthermore, microalgae-derived metabolites, including polyunsaturated fatty acids, carotenoids, and polysaccharides, play a pivotal role in suppressing the synthesis of pro-inflammatory mediators (Choo et al., 2020). These bioactive compounds inhibit the production of cytokines such as TNF-α, IL-1β, and IL-6, which are critical drivers of inflammation (Ávila-Román et al., 2021). Additionally, microalgae metabolites modulate the arachidonic acid pathway, reducing eicosanoid synthesis, including prostaglandins and leukotrienes (Harwood, 2023). This anti-inflammatory action occurs through the downregulation of NF-κB and COX-2 signaling pathways (Nabil-Adam et al., 2023; Talero et al., 2015). These metabolites offer potential therapeutic applications in managing chronic inflammatory conditions and promoting overall health by mitigating the inflammatory cascade effectively. In summary, the anti-inflammatory potential of microalgae represents a promising research domain, with several studies emphasizing the variety of bioactive chemicals generated by these microscopic entities.

Antimicrobial characteristics

Recent research indicates that microalgae contain distinctive bioactive chemicals that demonstrate significant antibacterial activity, presenting a viable alternative to conventional antimicrobial treatments (Ferrazzano et al., 2020). A multitude of studies has investigated the antibacterial properties of various microalgal species. Cyanobacteria and microalgae are recognized as prolific sources of diverse bioactive compounds, such as polyphenols, terpenoids, and carotenoids, which exhibit antimicrobial properties against several pathogenic bacteria (Ferrazzano et al., 2020; Mamani et al., 2020). Furthermore, Chlorella, Spirulina, and Dunaliella produce secondary metabolites, including peptides, polysaccharides, phenolics, and fatty acids, that exhibit potent antimicrobial properties (Ilieva et al., 2024; Rojas et al., 2020). The primary mechanism of action behind the antimicrobial effects of these compounds is to disrupt the integrity of microbial cell membranes (Stirk and van Staden, 2022). Additionally, fatty acids like polyunsaturated lipids and certain peptides in microalgae destabilize bacterial and fungal membranes, causing leakage of cellular contents and eventual cause cell death (Surendhiran et al., 2021). Moreover, microalgae-derived phenolics and flavonoids inhibited the activity of microbial enzymes disturb the metabolic pathways crucial to maintain the normal growth and multiplication of microbial cells (Hassan et al., 2022b). Another mechanism involved to inhibit the bacterial growth, microalgae produce ROS and antioxidant compounds (carotenoids and phycocyanin), that create oxidative stress within microbial cells, impairing DNA, proteins, and lipid integrity leading to cause cell death (Hamidi et al., 2019). In addition to the direct anti-microbial effects, microalgae also modulate gut microbiota by promoting beneficial microbial growth while suppressing pathogenic species (Ma et al., 2022). This competitive inhibition is attributed to the production of antimicrobial metabolites and improve the immunological status and gut barrier functions, thereby improving the health and proactive performance of livestock animals.

The antibacterial capabilities of microalgae can be affected by several factors, including growing conditions, extraction procedures, and specie of organism. A study on Spirulina platensis shown that the supercritical fluid extracts of this microalga displayed significant antibacterial activity against gram-positive and gram-negative bacteria, as well as yeasts and fungi (Mendiola et al., 2007). Similarly another study, demonstrated that microalgal species such as Chlorella, Dunaliella, and Nostoc produce bioactive chemicals having with superior antibacterial characteristics (Saha and Murray, 2018). The antibacterial capabilities of microalgae signify a viable direction for additional research and development by utilizing varied bioactive molecules generated by these photosynthetic organisms.

Advantageous Utilization of Microalgae in Poultry

Effect on growth performance

Microalgae possess considerable potential to enhance growth performance and general health in poultry (Table 2). These microorganisms exhibit an extraordinary capacity to flourish under diverse environmental settings, rendering them a versatile and sustainable feedstock alternative. Multiple studies have evidenced the beneficial effects of integrating microalgae into poultry feed on several growth metrics, including body weight, feed conversion ratio, and egg production (Benedetti et al., 2018; de Morais et al., 2016).

Table 2. Showing the beneficial effect of microalgae on poultry birds
Type of animal Type, dosage and duration Mechanism Overall effect References
Broilers and layers Spirulina (1.5%, 3.0%, 6.0%, or 12.0% for nine weeks ↑ Cellular and humoral immunity,
↑ Maintaining the beneficial intestinal bacteria
↓ Pathogenic bacteria
↑ Improving the carcass traits
Improves productive performance of broilers and layers El-Ghany (2020)
Broilers 1%–2% micro algae in diet for 42 days ↑ Superoxide dismutase (SOD)
↓ Polyunsaturated fatty acid
↓ Malondialdehyd
Improves performance, serum composition, carcass trait, antioxidant status, and fatty acid El-Bahr et al. (2020)
Broilers Microalgae Chlorella spp. 0.5%–1.0% of the diet ↑ Blood total protein, albumin
↑ High-density lipoprotein (HDL) cholesterol
↓ Alanine aminotransferase and ALT
↑ Blood lymphocytes
↑ IgA, IgG, and IgM
↑ Body weight gain
↓ Feed conversion ratio
↓ Drip loss
↑ Liver function
↑ Immunity
Abdelnour et al. (2019)
Cornish cross chicks Docosahexaenoic acid (DHA; 22:6n-3)-rich 2% microalgae for day 42 ↑ Breast muscle
↑ Meat tenderness and color
↓ Incidence of breast muscle striping and myopathy
Improves production performance, breast muscle quality attributes, lipid profile, and incidence of white striping and myopathy Khan et al. (2021)
Isa brown laying hens DHA-rich microalga 0.25%, 0.5%, and 1.0% for 40 d ↑ Nutrititive value of hen’s eggs ↑ Omega-3 content of eggs Moran et al (2018); Moran et al. (2019)
Broiler chickens Microalgae Tetraselmis chuii 20 g/kg of feed (2%) S. Infantis caecal load Antibacterial Corrales-Martinez et al. (2022)
Broiler chickens Microalgal DHA 2% for 6 weeks ↑ Body weight gain
↓ Cholesterol and triglyceride concentrations in plasma, liver, breast, and thigh
↑ Improve tibia breaking strength
↑ Total bone volume and bone mineral
Improves growth performance, tissue lipid profiles, and tibia characteristics Kalia et al. (2023)
Fayoumi broilers Microalgae (Spirulina platensis) 1% for 8 weeks ↑ Serum total protein
↑ Globulin
↓ Serum cholesterol
↑ Lymphocyte percentage
Improves growth performance, ingestive behavior, hemato-biochemical parameters, and economic efficiency Hassan et al. (2022a)
Broiler and layer birds Microalgae ↑ Weight, Feed intake and digestibility
↑ Increase meat quality
↑ Improve organoleptic quality of meat
↑ Digestibility
↑ Egg shell thickness and egg weight
Enhances the nutritive value of poultry meat an eggs Esakkimuthu et al. (2024)
Broiler and layer birds S. platensis (0.25%–1.0%) and Chlorella vulgaris (1.55 g/kg) ↓ Oxidative stress
↑ Immune response, growth rates, feed conversion ratios
↑ Carcass quality, and meat attributes
↑ Egg production and egg quality
Positive impact on performance metrics Abdel-Wareth et al. (2024)
Broiler S. platensis (10%) and Haematococcus pluvialis (0.004%) ↑ GSH, glutathione peroxidase (GPx) and SOD Improves antioxidant status Abdel-Wareth et al. (2024); Jubie et al. (2012)
Broilers C. vulgaris spp.; CLV; 0.5%–1.0% of the diet) ↑ Body weight gain (2.7%)
↑ Feed conversion ratio (lowered by 2.8%)
↑ Meat color and breast muscle weight (20.1%)
↓ Drip loss (2.26%) from breast muscle
↑ IgA (29.7%,), IgG (69.1%), and IgM (32.3%)
Improves growth and health of birds Abdelnour et al. (2019)
Ross-308 broiler chicks 1 g/kg diet of C. vulgaris (CV), S. platensis, and Amphora coffeaformis (AC) ↑ Essential fatty and amino acids
↓ Microbial growth in breast muscle
↓ Malondialdehyde (MDA) and protein carbonyl (PC) levels, cooking loss and aerobic plate count (APC)
↑ SOD activities in breast muscle
Enhance performance and meat quality in broiler chickens El-Bahr et al. (2020)
Download Excel Table

Three kinds of microalgae, namely C. vulgaris, S. platensis, and Amphora coffeaformis, were reported to positively influence body weight, growth performance, and meat quality in broiler chickens (El-Bahr et al., 2020). The results indicated that microalgae substantially enhanced the profiles of important fatty and amino acids, increased antioxidant levels in breast muscles, and diminished microbial development and oxidative damage (El-Bahr et al., 2020). Another study indicated that supplementing broiler diets with microalgae, with or without xylanase, markedly enhanced growth performance, increasing body weight by over 44% and decreasing feed conversion ratio by 6.3%. They further suggested possible advantages for gut health, evidenced by notable alterations in gut health genes and an expanded villi surface area in the microalgae groups (Chaudhary et al., 2023a). Another study examined the effects of S. platensis supplementation in Fayoumi hens, demonstrating that a diet containing 1% S. platensis markedly enhanced growth performance and immunological response. Economically, 0.25% S. platensis was determined to be the most cost-effective, optimizing production and profitability (Hassan et al., 2022a). Moreover, the pilot investigation indicated that food supplementation with Tetraselmis chuii and Porphyridium cruentum microalgae enhanced body weight and gut morphology in broiler chicks. Treated birds exhibited increased villus-height-to-crypt-depth ratios, less thawing weight loss in fillets, and higher nutrient absorption, indicating a viable approach for augmenting growth performance (Šefcová et al., 2021). Supplementation of heat-stressed broilers with 3% microalgae markedly increased final body weight and improved gut health indicators, encompassing antioxidant, immunological, and tight-junction gene expression. Furthermore, microalgae enhanced microbial diversity and fostered good gut bacteria, illustrating its potential to alleviate heat stress in chickens (Chaudhary et al., 2023b). Enhancing the diets of Arbor Acres chicks with DHA-enriched microalgae markedly enhanced growth performance, liver proportion, and antioxidant status, while decreasing abdominal fat and blood cholesterol levels. Furthermore, birds that consumed microalgae exhibited enhanced deposition of good fatty acids and decreased oxidative stress relative to the control group (Long et al., 2018). The published research demonstrates that microalgae is a significant and dependable feed element for enhancing the productive performance of chickens (Fig. 2).

kosfa-45-1-243-g2
Fig. 2. Illustrating the advantageous impact of microalgae on avian species. GPx, glutathione peroxidase; CAT, catalase; SOD, superoxide dismutase; MDA, malondialdehyde; ROS, reactive oxygen species; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; GST, glutathione S-transferase.
Download Original Figure
Effects on meat production and quality attributes

Integrating microalgae into poultry feed offers the significant benefit of potentially enhancing the nutritional quality of the meat (Martins et al., 2021). In addition, microalgae containing carotenoids and other bioactive compounds that can enhance the color and overall quality of poultry meat. Studies have shown that adding ω-3-rich microalgae (Schizochytrium JB5) to broiler diets improved the fatty acid composition of breast meat by increasing levels of DHA, oleic acid, and ω-3 fatty acids, while decreasing the ratio of ω-6 to ω-3 and the saturated fat content (Gatrell et al., 2015). Despite these advantages, the growth performance and blood parameters of the poultry were not impacted by the inclusion of microalgae in their diet (Yan and Kim, 2013). Furthermore, a research examined the impact of various microalgae species on broiler chickens. It demonstrated that S. platensis notably enhanced the crucial fatty and amino acid compositions while decreasing microbial growth in the breast muscle (Amer et al., 2024). In addition, all microalgae types decreased the markers of oxidative stress and enhanced meat quality by reducing melondialdehyde and protein carbonyl levels, as well as cooking loss (Varzaru et al., 2024). These results indicated that microalgae have the potential to enhance broiler performance and meat quality. On the contrary, a recent study on feeding trials examined the impact of incorporating microalgal biomass into broiler diets. The results revealed that substituting 5%–10% of soybean meal with three different microalgal strains led to a reduction in breast weight percentages, while not impacting the overall growth performance or meat quality (Cabrol et al., 2022). It is worth noting that the combined use of microalgae did not prevent the loss of breast weight and also influenced gene expressions associated with muscle hypertrophy and atrophy, indicating complex effects on protein metabolism (Sun et al., 2024). In addition, Liu and his collogues studied that laying hens fed diet supplemented with DHA-rich microalgae (Aurantiochytrium sp.) led to a significant enhancement in the n-3 polyunsaturated fatty acid levels and lipid health indicators of breast and thigh meat (Liu et al., 2022). The enrichment did not affect meat quality aspects such as tenderness or color, however slight increase in lipid oxidation was observed in cooked and stored meat (Liu et al., 2022). Furthermore, incorporating Hermetia illucens larval meal or spirulina into the poultry diet, showed slightly increase in color and saturated fat content (Gkarane et al., 2020). Similarly, another study reported that spirulina supplementation significantly improved the red color of chicken and enhance the umami flavor of meat after storage under oxygen-rich environment (Altmann et al., 2020). Furthermore, dietary incorporation of alternative protein sources such as Spirulina and Hermetia meal to poultry feed demonstrates encouraging outcomes for the quality of meat, especially when combined with advanced packaging techniques (Altmann, 2020). Moreover, broiler chicken diets enriched with DHA-rich microalgae and methionine led to a significant decrease in the occurrence of breast muscle white striping and myopathy, along with an improvement in the muscle’s n-3 fatty acid content (Khan et al., 2021). Nevertheless, the incorporation of methionine resulted in increased meat tenderness and changes in its color, suggesting possible trade-offs in meat quality (Khan et al., 2021). Conclusively, incorporating microalgae into poultry feeds has revealed a substantial potential and great promise in improving efficiency and supporting the creation of premium poultry goods.

Effect on egg production

Exploring the use of microalgae in poultry feed has been considered to enhance egg production, as these tiny organisms can provide important nutrients like proteins, lipids, and pigments (Fernandes et al., 2020a). C. vulgaris and S. platensis are an examples of microalgae that contain various bioactive compounds capable of positively impacting the health and performance of laying hens. Incorporating microalgae into poultry diets not only boosts egg production but also enhances the nutritional content and sensory characteristics of the eggs (Liu et al., 2020). The presence of abundant amount of carotenoids and fatty acids in microalgae biomass, significantly improve the eggs’ color, texture, and overall quality, making them more attractive to consumers (Kalia and Lei, 2022).

Research has shown that integrating microalgae into chicken feed can cause a notable rise in egg output. The active components found in microalgae, like carotenoids and polyunsaturated fatty acids, can boost the metabolic functions of the birds, improving nutrient absorption and energy effectiveness (Vlaicu et al., 2023). Additionally, superior nutritional value of microalgae helps to boost growth performance and optimize the development of reproductive system of laying hens leading to increased egg production (Martins et al., 2021). Preceding studies have shown that the active components in microalgae, like carotenoids and polyunsaturated fatty acids, can boost the metabolic functions of the birds, improving nutrient absorption and energy effectiveness (Emam et al., 2024). In addition, the supplementation of S. platensis to the feed for layers resulted in noticeable enhancements in egg production, egg quality, and indicators of blood health (Abbas et al., 2022). The most effective level of S. platensis inclusion was found to be 9%, with 4.7% of soybean meal being replaced for every 1% of S. platensis, indicating its viability as a cost-effective dietary alternative (Abbas et al., 2022).

During a 32-week experiment, the addition of graded levels of All-G-RichTM microalgae in layer diets resulted in a notable elevation of DHA levels in egg yolks, with no impact on production performance, egg weight, or shell quality (Ao et al., 2015; Keegan et al., 2019). Simultaneously, dietary supplementation of microalgae oil or fish oil to the diet of laying hens raised DHA levels and n-3 PUFA in eggs, encouragingly both sources were found equally effective (Kaur et al., 2024). Nevertheless, eggs produced from microalgae oil had a better taste and were more generally accepted, indicating that it could be a more favorable choice for enriching DHA compared to fish oil (Feng et al., 2020). Likewise, the addition of omega-3-rich microalgae such as Phaeodactylum tricornutum, Isochrysis galbana, and Chlorella fusca to the diets of laying hens resulted in a significant increase in n-3 long-chain polyunsaturated fatty acids (LC-PUFA) in egg yolk, particularly DHA (Lemahieu et al., 2013). It is important to note that C. fusca mainly boosted α-linolenic acid, while Phaeodactylum and Isochrysis demonstrated the highest LC-PUFA efficiency, also improving yolk color through carotenoid transfer (Lemahieu et al., 2013). Whereas another study demonstrated that enhancing the diets of Japanese quail with Spirulina and Dunaliella (SD) resulted in better body weight, feed conversion ratio, and fertility, along with remarkable decreases in lipid profile indicators (Abd El-Hack et al., 2024). Despite minimal changes in egg production and quality, the use of SD improved the function of the liver and kidneys, as well as the quails’ immunological response (Abd El-Hack et al., 2024). Convincingly, it was noted that adding microalgae to the diet not only enhances egg production but also elevates the nutritional quality of poultry eggs.

Potential Drawbacks of Adding Microalgae to Poultry Feed

The widespread use of microalgae in poultry diets has been impeded by various constraints that require significant attention. A key obstacle is the inconsistent quality and makeup of microalgae, which can be impacted by several factors like cultivation conditions, harvesting methods, and processing techniques (Martins et al., 2021). Henceforth, formulating poultry diets that consistently meet the birds’ specific nutritional requirements can be challenging due to the variability in ingredients. Additionally, the high expense of producing and processing microalgae may render it economically impractical for large-scale commercial poultry operations, particularly when compared to traditional protein sources like soybean meal and fishmeal (Ciani et al., 2021; Sanjari et al., 2018).

Microalgae’s potential to cause unwanted sensory characteristics in poultry products, such as off-flavors or texture alterations, presents another limitation (Espinosa-Ramírez et al., 2023). This limitation can significantly hinder consumer acceptance, especially for eggs and meat, which are highly sensitive to flavor and quality. Furthermore, incorporating microalgae into poultry diets can be difficult due to the requirement for specialized feed processing equipment and the possibility of decreased feed intake or digestibility in the birds. Despite these constraints, continuous research and technological progress could potentially surmount the obstacles to the extensive utilization of microalgae in poultry nutrition. Innovative methods of cultivation, such as utilizing wastewater or industrial waste streams as nutrient sources, may aid in cutting production expenses and enhancing the sustainability of feeds based on microalgae.

Conclusion

Microalgae holds significant potential as a nutraceutical and alternative protein source for the poultry industry, offering a sustainable, nutrient-rich solution to enhance poultry health and productivity. It is widely accepted that microalgae are a valuable source of essential nutrients, such as proteins, omega-3 fatty acids, vitamins, and antioxidants, which help to boost immune status, enhance nutrient utilization, reduce oxidative stress and prevent infectious disorders, thereby improves health status and overall productive performance. Furthermore, microalgae contribute to gut health by modulating gut microbiota and improving intestinal integrity, thus decreasing the incidence of diseases. Additionally, inclusion of microalgae in poultry diets significantly enhance quality of meat and egg by improving the nutrient content and reducing undesirable fatty acids, these benefits make them a valuable feed additive for modern poultry to ensure the consistent productivity.

Conflicts of Interest

The authors declare no potential conflicts of interest.

Acknowledgements

This research was supported by the Fundamental Reserach Funds for the Central Universities (31920230192), and the Qinghai Fundamental Scientific and Technological Research Plan (2023-ZJ-783).

Author Contributions

Conceptualization: Zhang LX, Jiang YN. Formal analysis: Ahmed S, Li CX. Methodology: Ma LN. Software: Buzdar JA, Ahmed S, Li FH, Ma LN. Validation: Sun XY, Wu PF, Li CX. Investigation: Buzdar JA, Sun XY, Li FH, Wu PF. Writing - original draft: Zhang LX, Jiang YN. Writing - review & editing: Zhang LX, Jiang YN, Buzdar JA, Ahmed S, Sun XY, Li FH, Ma LN, Wu PF, Li CX.

Ethics Approval

This article does not require IRB/IACUC approval because there are no human and animal participants.

References

1.

Abbas AO, Alaqil AA, Mehaisen GMK, Kamel NN. 2022; Effect of dietary blue-green microalgae inclusion as a replacement to soybean meal on laying hens’ performance, egg quality, plasma metabolites, and hematology. Animals. 12:2816

2.

Abd El-Hack ME, Majrashi KA, Fakiha KG, Roshdy M, Kamal M, Saleh RM, Khafaga AF, Othman SI, Rudayni HA, Allam AA. 2024; Effects of varying dietary microalgae levels on performance, egg quality, fertility, and blood biochemical parameters of laying Japanese quails (Coturnix coturnixJaponica). Poult Sci. 103:103454

3.

Abdel-Wareth AAA, Williams AN, Salahuddin M, Gadekar S, Lohakare J. 2024; Algae as an alternative source of protein in poultry diets for sustainable production and disease resistance: Present status and future considerations. Front Vet Sci. 11:1382163

4.

Abdelnour SA, Abd El-Hack ME, Arif M, Khafaga AF, Taha AE. 2019; The application of the microalgae Chlorella spp. as a supplement in broiler feed. World’s Poult Sci J. 75:305-318

5.

Aboamer AA, Ebeid HM, Siddique F, Arain MA, Hassan F. 2024 Nutraceutical potential of essential oils in dairy animal diets: Challenges and opportunities. Proc Indian Natl Sci Acad (in press). doi:

6.

Alfaia CM, Pestana JM, Rodrigues M, Coelho D, Aires M, Ribeiro DM, Major VT, Martins CF, Santos H, Lopes PA. 2021; Influence of dietary Chlorella vulgaris and carbohydrate-active enzymes on growth performance, meat quality and lipid composition of broiler chickens. Poult Sci. 100:926-937

7.

Alghamdi MA, Elbaz MI, Ismail IE, Reda FM, Alagawany M, El-Tarabily KA, Abdelgeliel AS. 2024; Dietary supplementation with a mixture of Dunaliella salina and Spirulina enhances broiler performance by improving growth, immunity, digestive enzymes and gut microbiota. Poult Sci. 103:103337

8.

Alghazeer R, El Fatah H, Azwai S, Elghmasi S, Sidati M, El Fituri A, Althaluti E, Gammoudi F, Yudiati E, Talouz N, Shamlan G, AL-Farga A, Alansari WS, Eskandrani AA. 2022; Nutritional and nonnutritional content of underexploited edible seaweeds. Aquacult Nutr. 2022:8422414

9.

Altmann BA. 2020 The meat science perspective of spirulina (Arthrospira platensis) and black soldier fly larvae (Hermetia illucens) as alternative protein feeds in broiler and swine production. Ph.D. dissertation. Georg-August Univ. Göttingen, Germany: .

10.

Altmann BA, Wigger R, Ciulu M, Mörlein D. 2020; The effect of insect or microalga alternative protein feeds on broiler meat quality. J Sci Food Agric. 100:4292-4302

11.

Amer SA, Behairy A, Moustafa AA, Eltanahy A, Younis EM, Abdel-Warith AWA, Osman A, Gouda A, Davies SJ, Tolba SA. 2024 Effects of dietary Arthrospira platensis phycocyanin on growth, fatty acid assessment of breast muscles, hematobiochemical, immunological responses, and hepatic histomorphology in broiler chickens. J Appl Phycol (in press). doi:

12.

Ao T, Macalintal LM, Paul MA, Pescatore AJ, Cantor AH, Ford MJ, Timmons B, Dawson KA. 2015; Effects of supplementing microalgae in laying hen diets on productive performance, fatty-acid profile, and oxidative stability of eggs. J Appl Poult Res. 24:394-400

13.

Arain MA, Khaskheli GB, Barham GS, Marghazani IB. 2024; Lactoferrin’s role in modulating NF-κB pathway to alleviate diabetes-associated inflammation: A novel in-silico study. Heliyon. 10e34051

14.

Arain MA, Mei Z, Hassan FU, Saeed M, Alagawany M, Shar AH, Rajput IR. 2018; Lycopene: A natural antioxidant for prevention of heat-induced oxidative stress in poultry. World’s Poult Sci J. 74:89-100

15.

Arain MA, Nabi F, Marghazani IB, Hassan F, Soomro H, Kalhoro H, Soomro F, Buzdar JA. 2022a; In ovo delivery of nutraceuticals improves health status and production performance of poultry birds: A review. World’s Poult Sci J. 78:765-788

16.

Arain MA, Nabi F, Shah QA, Alagawany M, Fazlani SA, Khalid M, Soomro F, Khand FM, Farag MR. 2022b; The role of early feeding in improving performance and health of poultry: Herbs and their derivatives. World’s Poult Sci J. 78:499-513

17.

Araj-Shirvani M, Honarvar M, Jahadi M, Mizani M. 2024; Biochemical profile of Dunaliella isolates from different regions of Iran with a focus on pharmaceutical and nutraceutical potential applications. Food Sci Nutr. 12:4914-4926

18.

Arif M, Rehman A, Saeed M, El-Hack MEA, Alagawany M, Abbas H, Arian MA, Fazlani SA, Hussain AI, Ayaşan T. 2017; Effect of different processing methods of pigeon pea (Cajanus cajan) on growth performance, carcass traits, and blood biochemical and hematological parameters of broiler chickens. Turk J Vet Anim Sci. 41:38-45

19.

Ashraf MF, Zubair D, Bashir MN, Alagawany M, Ahmed S, Shah QA, Buzdar JA, Arain MA. 2024; Nutraceutical and health-promoting potential of lactoferrin, an iron-binding protein in human and animal: Current knowledge. Biol Trace Elem Res. 202:56-72

20.

Ávila-Román J, García-Gil S, Rodríguez-Luna A, Motilva V, Talero E. 2021; Anti-inflammatory and anticancer effects of microalgal carotenoids. Mar Drugs. 19:531

21.

Balakrishnan J, Ganapathi P, Kannan S, Marudhamuthu M, Shanmugam K. 2021; Anti-listerial activity of microalgal fatty acid methyl esters and their possible applications as chicken marinade. Int J Food Microbiol. 339:109027

22.

Bature A, Melville L, Rahman KM, Aulak P. 2022; Microalgae as feed ingredients and a potential source of competitive advantage in livestock production: A review. Livest Sci. 259:104907

23.

Behan AA, Ahmed S, Hassan MF, Buzdar JA, Shah QA, Khan KA, Arain MA. 2024 Nutritional and health beneficial application of lactoferrin in some animal species: An updated review. Proc Indian Natl Sci Acad (in press). doi:

24.

Benedetti M, Vecchi V, Barera S, Dall’Osto L. 2018; Biomass from microalgae: The potential of domestication towards sustainable biofactories. Microb Cell Fact. 17:1-18

25.

Bergamini CM, Gambetti S, Dondi A, Cervellati C. 2004; Oxygen, reactive oxygen species and tissue damage. Curr Pharm Des. 10:1611-1626

26.

Bhuvana P, Sangeetha P, Anuradha V, Ali MS. 2019; Spectral characterization of bioactive compounds from microalgae: N. oculata and C. vulgaris. Biocatal Agric Biotechnol. 19:101094

27.

Cabrol MB, Martins JC, Malhão LP, Alves SP, Bessa RJB, Almeida AM, Raymundo A, Lordelo M. 2022; Partial replacement of soybean meal with Chlorella vulgaris in broiler diets influences performance and improves breast meat quality and fatty acid composition. Poult Sci. 101:101955

28.

Castro-Varela PA, Celis-Plá PSM, Abdala-Díaz R, Figueroa FL. 2021; Photobiological effects on biochemical composition in Porphyridium cruentum (Rhodophyta) with a biotechnological application. Photochem Photobiol. 97:1032-1042

29.

Chang CWT, Takemoto JY, Chang PE, AlFindee MN, Lin YY. 2021; Effects of mesobiliverdin IXα-enriched microalgae feed on gut health and microbiota of broilers. Front Vet Sci. 7:586813

30.

Changxing L, Chenling M, Alagawany M, Jianhua L, Dongfang D, Gaichao W, Wenyin Z, Syed SF, Arain MA, Saeed M. 2018; Health benefits and potential applications of anthocyanins in poultry feed industry. World’s Poult Sci J. 74:251-264

31.

Chaudhary A, Mishra P, Al Amaz S, Mahato PL, Das R, Jha R, Mishra B. 2023a; Dietary supplementation of microalgae mitigates the negative effects of heat stress in broilers. Poult Sci. 102:102958

32.

Chaudhary P, Janmeda P, Docea AO, Yeskaliyeva B, Abdull Razis AF, Modu B, Calina D, Sharifi-Rad J. 2023b; Oxidative stress, free radicals and antioxidants: Potential crosstalk in the pathophysiology of human diseases. Front Chem. 11:1158198

33.

Chen M, Chen Y, Zhang Q. 2024; Assessing global carbon sequestration and bioenergy potential from microalgae cultivation on marginal lands leveraging machine learning. Sci Total Environ. 948:174462

34.

Chia MA, Lombardi AT, Melão MGG, Parrish CC. 2015; Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquat Toxicol. 160:87-95

35.

Choo WT, Teoh ML, Phang SM, Convey P, Yap WH, Goh BH, Beardall J. 2020; Microalgae as potential anti-inflammatory natural product against human inflammatory skin diseases. Front Pharmacol. 11:1086

36.

Ciani M, Lippolis A, Fava F, Rodolfi L, Niccolai A, Tredici MR. 2021; Microbes: Food for the future. Foods. 10:971

37.

Cirulis JT, Scott JA, Ross GM. 2013; Management of oxidative stress by microalgae. Can J Physiol Pharmacol. 91:15-21

38.

Clonan A, Roberts KE, Holdsworth M. 2016; Socioeconomic and demographic drivers of red and processed meat consumption: Implications for health and environmental sustainability. Proc Nutr Soc. 75:367-373

39.

Conde TA, Zabetakis I, Tsoupras A, Medina I, Costa M, Silva J, Neves B, Domingues P, Domingues MR. 2021; Microalgal lipid extracts have potential to modulate the inflammatory response: A critical review. Int J Mol Sci. 22:9825

40.

Corrales-Martinez J, Ortega-Paredes D, Šefcová MA, Larrea-Álvarez CM, de Janon S, Medina-Santana J, Molina-Cuasapaz G, Vinueza-Burgos C, Revajová V, Larrea-Álvarez M, Calero-Cáceres W. 2022; A PMAxxTM qPCR assay reveals that dietary administration of the microalgae Tetraselmis chuii does not affect Salmonella infantis caecal content in early-treated broiler chickens. Vet Sci. 9:487

41.

Coulombier N, Jauffrais T, Lebouvier N. 2021; Antioxidant compounds from microalgae: A review. Mar Drugs. 19:549

42.

Darwish R, Gedi MA, Akepach P, Assaye H, Zaky AS, Gray DA. 2020; Chlamydomonas reinhardtii is a potential food supplement with the capacity to outperform Chlorella and Spirulina. Appl Sci. 10:6736

43.

de Morais EG, Moraes L, de Morais MG, Costa JAV. 2016; Biodiesel and bioethanol from microalgae. In Green fuels technology: Biofuels. In: Soccol C, Brar S, Faulds C, Ramos L, editors.(ed)Springer. Cham, Switzerland: pp p. 359-386

44.

de Morais MG, Vaz BS, de Morais EG, Costa JAV. 2015; Biologically active metabolites synthesized by microalgae. BioMed Res Int. 2015:835761

45.

Demirel Z. 2022; Monitoring of growth and biochemical composition of Dunaliella salina and Dunaliella polymorpha in different photobioreactors. Aquat Res. 5:136-145

46.

Dineshkumar R, Narendran R, Jayasingam P, Sampathkumar P. 2017; Cultivation and chemical composition of microalgae Chlorella vulgaris and its antibacterial activity against human pathogens. J Aquac Mar Biol. 5:00119

47.

Dolganyuk V, Belova D, Babich O, Prosekov A, Ivanova S, Katserov D, Patyukov N, Sukhikh S. 2020; Microalgae: A promising source of valuable bioproducts. Biomolecules. 10:1153

48.

Du H, Sarwar I, Ahmad S, Suheryani I, Anjum S, Andlib S, Kakar MU, Arain MA. 2024; Organic acids in poultry industry: A review of nutritional advancements and health benefits. World’s Poult Sci J. 80:133-153

49.

El-Bahr S, Shousha S, Shehab A, Khattab W, Ahmed-Farid O, Sabike I, El-Garhy O, Albokhadaim I, Albosadah K. 2020; Effect of dietary microalgae on growth performance, profiles of amino and fatty acids, antioxidant status, and meat quality of broiler chickens. Animals. 10:761

50.

El-Ghany WAA. 2020; Microalgae in poultry field: A comprehensive perspectives. Adv Anim Vet Sci. 8:888-897

51.

Emam KRS, Ali SAM, Morsy AS, Fouda WA, Elbaz AM. 2024; Role of Nannochloropsis oculata supplement in improving performance, antioxidant status, blood metabolites, and egg quality of laying hens under hot environmental conditions. Sci Rep. 14:16884

52.

Esakkimuthu S, Siddiqui SA, Cherif M, Saadaoui I. 2024; Exploring strategies to enhance microalgae nutritional quality for functional poultry-sourced food products. Bioresour Technol Rep. 25:101746

53.

Espinosa-Ramírez J, Mondragón-Portocarrero AC, Rodríguez JA, Lorenzo JM, Santos EM. 2023; Algae as a potential source of protein meat alternatives. Front Nutr. 10:1254300

54.

Feng J, Long S, Zhang H, Wu S, Qi G, Wang J. 2020; Comparative effects of dietary microalgae oil and fish oil on fatty acid composition and sensory quality of table eggs. Poult Sci. 99:1734-1743

55.

Fernandes RTV, Gonçalves AA, Arruda AMV. 2020a; Production, egg quality, and intestinal morphometry of laying hens fed marine microalga. Rev Bras Zootec. 49e20200011

56.

Fernandes T, Fernandes I, Andrade CAP, Cordeiro N. 2020b; Assessing the impact of sulfur concentrations on growth and biochemical composition of three marine microalgae. J Appl Phycol. 32:967-975

57.

Ferrazzano GF, Papa C, Pollio A, Ingenito A, Sangianantoni G, Cantile T. 2020; Cyanobacteria and microalgae as sources of functional foods to improve human general and oral health. Molecules. 25:5164

58.

Ferreira AF, Ferreira A, Dias APS, Gouveia L. 2020; Pyrolysis of Scenedesmus obliquus biomass following the treatment of different wastewaters. BioEnergy Res. 13:896-906

59.

Gatrell SK, Kim J, Derksen TJ, O’Neil EV, Lei XG. 2015; Creating ω-3 fatty-acid-enriched chicken using defatted green microalgal biomass. J Agric Food Chem. 63:9315-9322

60.

Gauthier MR, Senhorinho GNA, Scott JA. 2020; Microalgae under environmental stress as a source of antioxidants. Algal Res. 52:102104

61.

Gkarane V, Ciulu M, Altmann BA, Schmitt AO, Mörlein D. 2020; The effect of algae or insect supplementation as alternative protein sources on the volatile profile of chicken meat. Foods. 9:1235

62.

Gržinić G, Piotrowicz-Cieślak A, Klimkowicz-Pawlas A, Górny RL, Ławniczek-Wałczyk A, Piechowicz L, Olkowska E, Potrykus M, Tankiewicz M, Krupka M, Siebielec G, Wolska L. 2023; Intensive poultry farming: A review of the impact on the environment and human health. Sci Total Environ. 858:160014

63.

Hamidi M, Kozani PS, Kozani PS, Pierre G, Michaud P, Delattre C. 2019; Marine bacteria versus microalgae: Who is the best for biotechnological production of bioactive compounds with antioxidant properties and other biological applications?. Mar Drugs. 18:28

64.

Hamouda RA, Abd El Latif A, Elkaw EM, Alotaibi AS, Alenzi AM, Hamza HA. 2022; Assessment of antioxidant and anticancer activities of microgreen alga Chlorella vulgaris and its blend with different vitamins. Molecules. 27:1602

65.

Harwood JL. 2023; Polyunsaturated fatty acids: Conversion to lipid mediators, roles in inflammatory diseases and dietary sources. Int J Mol Sci. 24:8838

66.

Hassan F, Liu C, Mehboob M, Bilal RM, Arain MA, Siddique F, Chen F, Li Y, Zhang J, Shi P, Lv B, Lin Q. 2023; Potential of dietary hemp and cannabinoids to modulate immune response to enhance health and performance in animals: Opportunities and challenges. Front Immunol. 14:1285052

67.

Hassan RIM, Refaie MS, El-Shoukary RD, Rehan IF, Zigo F, Karaffová V, Amer HY. 2022a; Effect of dietary microalgae (Spirulina platensis) on growth performance, ingestive behavior, hemato-biochemical parameters, and economic efficiency of Fayoumi broilers. Life. 12:1892

68.

Hassan S, Meenatchi R, Pachillu K, Bansal S, Brindangnanam P, Arockiaraj J, Kiran GS, Selvin J. 2022b; Identification and characterization of the novel bioactive compounds from microalgae and cyanobacteria for pharmaceutical and nutraceutical applications. J Basic Microbiol. 62:999-1029

69.

Ilieva Y, Zaharieva MM, Najdenski H, Kroumov AD. 2024; Antimicrobial activity of Arthrospira (former Spirulina) and Dunaliella related to recognized antimicrobial bioactive compounds. Int J Mol Sci. 25:5548

70.

Jubie S, Ramesh PN, Dhanabal P, Kalirajan R, Muruganantham N, Antony AS. 2012; Synthesis, antidepressant and antimicrobial activities of some novel stearic acid analogues. Eur J Med Chem. 54:931-935

71.

Kalia S, Lei XG. 2022; Dietary microalgae on poultry meat and eggs: Explained versus unexplained effects. Curr Opin Biotechnol. 75:102689

72.

Kalia S, Magnuson AD, Sun T, Liu G, Kim WK, Johnson Z, Lei XG. 2023; Supranutrition of microalgal docosahexaenoic acid and calcidiol improved growth performance, tissue lipid profiles, and tibia characteristics of broiler chickens. J Anim Sci Biotechnol. 14:27

73.

Kaur M, Shitanaka T, Surendra KC, Khanal SK. 2024 Macroalgae-derived bioactive compounds for functional food and pharmaceutical applications: A critical review. Crit Rev Food Sci Nutr (in press). doi:

74.

Keegan JD, Currie D, Knox A, Moran CA. 2019; Heterotrophic Aurantiochytrium sp. supplementation to layer diets sustainably increases the omega-3 concentration of eggs. Br Poult Sci. 60:570-578

75.

Khan FA, Almohazey D, Alomari M, Almofty SA. 2018; Isolation, culture, and functional characterization of human embryonic stem cells: Current trends and challenges. Stem Cells Int. 2018:1429351

76.

Khan IA, Parker NB, Löhr CV, Cherian G. 2021; Docosahexaenoic acid (22:6 n-3)-rich microalgae along with methionine supplementation in broiler chickens: Effects on production performance, breast muscle quality attributes, lipid profile, and incidence of white striping and myopathy. Poult Sci. 100:865-874

77.

Kiran BR, Venkata Mohan S. 2021; Microalgal cell biofactory: Therapeutic, nutraceutical and functional food applications. Plants. 10:836

78.

Koyande AK, Chew KW, Rambabu K, Tao Y, Chu DT, Show PL. 2019; Microalgae: A potential alternative to health supplementation for humans. Food Sci Hum Wellness. 8:16-24

79.

Laos FAS, Santa María SL, Campos MAV, Orellana SHC. 2023; Caulerpa filiformis (Suhr) hering una nueva opción antibacteriana. Rev Cubana Farm. 56e858.

80.

Lemahieu C, Bruneel C, Termote-Verhalle R, Muylaert K, Buyse J, Foubert I. 2013; Impact of feed supplementation with different omega-3 rich microalgae species on enrichment of eggs of laying hens. Food Chem. 141:4051-4059

81.

Lingala S, Freymond M, Tshering PP, Kumari P, Kraemer K, Beesabathuni K. 2024; The egg hub model: A sustainable and replicable approach to address food security and improve livelihoods. Curr Dev Nutr. 8:103795

82.

Liu B, Zhou Q, Zhu J, Lin G, Yu D, Ao T. 2020; Time course of nutritional and functional property changes in egg yolk from laying hens fed docosahexaenoic acid-rich microalgae. Poult Sci. 99:4616-4625

83.

Liu Y, Ren X, Fan C, Wu W, Zhang W, Wang Y. 2022; Health benefits, food applications, and sustainability of microalgae-derived N-3 PUFA. Foods. 11:1883

84.

Lobus NV, Kulikovskiy MS. 2023; The co-evolution aspects of the biogeochemical role of phytoplankton in aquatic ecosystems: A review. Biology. 12:92

85.

Long SF, Kang S, Wang QQ, Xu YT, Pan L, Hu JX, Li M, Piao XS. 2018; Dietary supplementation with DHA-rich microalgae improves performance, serum composition, carcass trait, antioxidant status, and fatty acid profile of broilers. Poult Sci. 97:1881-1890

86.

Lucas M, Freitas M, Carvalho F, Fernandes E, Ribeiro D. 2020; Antioxidant and pro-oxidant activities of carotenoids. In Plant antioxidants and health. In: Ekiert HM, Ramawat KG, Arora J, editors.(ed)Springer. Cham, Switzerland: pp p. 1-27

87.

Ma K, Chen S, Wu Y, Ma Y, Qiao H, Fan J, Wu H. 2022; Dietary supplementation with microalgae enhances the zebrafish growth performance by modulating immune status and gut microbiota. Appl Microbiol Biotechnol. 106:773-788

88.

Madeira MS, Cardoso C, Lopes PA, Coelho D, Afonso C, Bandarra NM, Prates JAM. 2017; Microalgae as feed ingredients for livestock production and meat quality: A review. Livest Sci. 205:111-121

89.

Madkour DM, Shapiai MI, Mohamad SE, Aly HH, Ismail ZH, Ibrahim MZ. 2023; A systematic review of deep learning microalgae classification and detection. IEEE Access. 11:57529-57555

90.

Maltsev Y, Maltseva K. 2021; Fatty acids of microalgae: Diversity and applications. Rev Environ Sci Biotechnol. 20:515-547

91.

Mamani J, Chávez J, Apumayta E, Gil-Kodaka P. 2020; Antioxidant activity and total phenolic content in Caulerpa filiformis (Chlorophyta) from Sechura Bay and Paracas Bay, Peru. Rev Peru Biol. 27:061-066

92.

Marinho YF, Malafaia CB, De Araújo KS, da Silva TD, dos Santos APF, de Moraes LB, Gálvez AO. 2021; Evaluation of the influence of different culture media on growth, life cycle, biochemical composition, and astaxanthin production in Haematococcus pluvialis. Aquacult Int. 29:757-778

93.

Markou G, Kougia E, Arapoglou D, Chentir I, Andreou V, Tzovenis I. 2023; Production of Arthrospira platensis: Effects on growth and biochemical composition of long-term acclimatization at different salinities. Bioengineering. 10:233

94.

Martínez-Francés E, Escudero-Oñate C. 2018; Cyanobacteria and microalgae in the production of valuable bioactive compounds. In Microalgal biotechnology. In: Jacob-Lopes E, Zepka LQ, Queiroz MI, editors.(ed)IntechOpen. London, UK: pp p. 104-128

95.

Martins CF, Ribeiro DM, Costa M, Coelho D, Alfaia CM, Lordelo M, Almeida AM, Freire JPB, Prates JAM. 2021; Using microalgae as a sustainable feed resource to enhance quality and nutritional value of pork and poultry meat. Foods. 10:2933

96.

Masojídek J, Torzillo G. 2014; Mass cultivation of freshwater microalgae. In Encyclopedia of Ecology. In: Jørgensen SE, Fath BD, editors.(ed)Academic Press. Cambridge, MA, USA: pp p. 2226-2235

97.

Mendiola JA, Jaime L, Santoyo S, Reglero G, Cifuentes A, Ibañez E, Señoráns FJ. 2007; Screening of functional compounds in supercritical fluid extracts from Spirulina platensis. Food Chem. 102:1357-1367

98.

Mnisi CM, Oyeagu CE, Akuru EA, Ruzvidzo O, Lewu FB. 2023; Sorghum, millet and cassava as alternative dietary energy sources for sustainable quail production: A review. Front Anim Sci. 4:1066388

99.

Mobin S, Alam F. 2017; Some promising microalgal species for commercial applications: A review. Energy Procedia. 110:510-517

100.

Moran CA, Currie D, Keegan JD, Knox A. 2018; Tolerance of broilers to dietary supplementation with high levels of the DHA-rich microalga, Aurantiochytrium limacinum: Effects on health and productivity. Animals. 8:180

101.

Moran CA, Morlacchini M, Keegan JD, Fusconi G. 2019; Increasing the omega-3 content of hen’s eggs through dietary supplementation with Aurantiochytrium limacinum microalgae: Effect of inclusion rate on the temporal pattern of docosahexaenoic acid enrichment, efficiency of transfer, and egg characteristics. J Appl Poult Res. 28:329-338

102.

Mottet A, Tempio G. 2017; Global poultry production: Current state and future outlook and challenges. World’s Poult Sci J. 73:245-256

103.

Munaro D, Nunes A, Schmitz C, Bauer C, Coelho DS, Oliveira ER, Yunes RA, Moura S, Maraschin M. 2021; Metabolites produced by macro- and microalgae as plant biostimulants. In Studies in natural products chemistry. In: (ed)Elsevier. Amsterdam, The Netherlands: pp p. 87-120

104.

Nabi F, Arain M, Hassan F, Umar M, Rajput N, Alagawany M, Syed SF, Soomro J, Somroo F, Liu J. 2020a; Nutraceutical role of selenium nanoparticles in poultry nutrition: A review. World’s Poult Sci J. 76:459-471

105.

Nabi F, Arain MA, Hassan MF, Shah QA, Almutairi MH, Buzdar JA. 2024; Effects of in ovo supplementation of selenium (Se) and zinc (zn) on hatchability and production performance of broiler chickens. J Comp Physiol B. 194:887-897

106.

Nabi F, Arain MA, Rajput N, Alagawany M, Soomro J, Umer M, Soomro F, Wang Z, Ye R, Liu J. 2020b; Health benefits of carotenoids and potential application in poultry industry: A review. J Anim Physiol Anim Nutr. 104:1809-1818

107.

Nabil-Adam A, Ashour ML, Shreadah MA. 2023; Modulation of MAPK/NF-κB pathway and NLRP3 inflammasome by secondary metabolites from red algae: A mechanistic study. ACS omega. 8:37971-37990

108.

Niccolai A, Zittelli GC, Rodolfi L, Biondi N, Tredici MR. 2019; Microalgae of interest as food source: Biochemical composition and digestibility. Algal Res. 42:101617

109.

Novoveská L, Nielsen SL, Eroldoğan OT, Haznedaroglu BZ, Rinkevich B, Fazi S, Robbens J, Vasquez M, Einarsson H. 2023; Overview and challenges of large-scale cultivation of photosynthetic microalgae and cyanobacteria. Mar Drugs. 21:445

110.

Pagels F, Amaro HM, Tavares TG, Amil BF, Guedes AC. 2022; Potential of microalgae extracts for food and feed supplementation: A promising source of antioxidant and anti-inflammatory compounds. Life. 12:1901

111.

Panaite TD, Cornescu GM, Predescu NC, Cismileanu A, Turcu RP, Saracila M, Soica C. 2023; Microalgae (Chlorella vulgaris and Spirulina platensis) as a protein alternative and their effects on productive performances, blood parameters, protein digestibility, and nutritional value of laying hens’ egg. Appl Sci. 13:10451

112.

Quintas-Nunes F, Brandão PR, Barreto Crespo MT, Glick BR, Nascimento FX. 2023; Plant growth promotion, phytohormone production and genomics of the rhizosphere-associated microalga, Micractinium rhizosphaerae sp. nov.. Plants. 12:651

113.

Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K. 2014; Oxidative stress, prooxidants, and antioxidants: The interplay. BioMed Res Int. 2014:761264

114.

Rendón-Castrillón L, Ramírez-Carmona M, Ocampo-López C, Giraldo-Aristizabal R. 2020; Evaluation of the operational conditions in the production and morphology of Chlorella sp. Braz J Biol. 81:202-209

115.

Ricky R, Chiampo F, Shanthakumar S. 2022; Efficacy of ciprofloxacin and amoxicillin removal and the effect on the biochemical composition of Chlorella vulgaris. Bioengineering. 9:134

116.

Rock KL, Latz E, Ontiveros F, Kono H. 2009; The sterile inflammatory response. Annu Rev Immunol. 28:321-342

117.

Rojas V, Rivas L, Cárdenas C, Guzmán F. 2020; Cyanobacteria and eukaryotic microalgae as emerging sources of antibacterial peptides. Molecules. 25:5804

118.

Saber AA, El-Refaey AA, Saber H, Singh P, van Vuuren SJ, Cantonati M. 2022; Cyanoprokaryotes and algae: Classification and habitats. In Handbook of algal biofuels. Aspects of cultivation, conversion, and biorefinery. In: El-Sheekh M, Abomohra AE, editors.(ed)Elsevier. Amsterdam, The Netherlands: pp p. 1-38

119.

Saeed M, Babazadeh D, Naveed M, Alagawany M, Abd El-Hack ME, Arain MA, Tiwari R, Sachan S, Karthik K, Dhama K, Elnesr SS, Chao S. 2019; In ovo delivery of various biological supplements, vaccines and drugs in poultry: Current knowledge. J Sci Food Agric. 99:3727-3739

120.

Saeed M, Babazadeh D, Naveed M, Arain MA, Hassan FU, Chao S. 2017a; Reconsidering betaine as a natural anti-heat stress agent in poultry industry: A review. Trop Anim Health Prod. 49:1329-1338

121.

Saeed M, Kalhoro SA, Naveed M, Hassan FU, Umar M, Rashid M, Memon SA, Soomro F, Arain MA, Chao S. 2018; Prospects of royal jelly as a potential natural feed additive in poultry diets. World’s Poult Sci J. 74:499-508

122.

Saeed M, Naveed M, Arain MA, Arif M, Abd El-Hack ME, Alagawany M, Siyal FA, Soomro RN, Sun C. 2017b; Quercetin: Nutritional and beneficial effects in poultry. World’s Poult Sci J. 73:355-364

123.

Safdar M, Hassan F, Khan MS, Hassan Khan A, Junejo Y, Ozaslan M, Arain MA, Behan AA. 2024; In silico analysis of polyphenols modulate bovine PPARγ to increase milk fat synthesis in dairy cattle via the MAPK signaling pathways. J Anim Sci. 102:skae248

124.

Saha SK, Murray P. 2018; Exploitation of microalgae species for nutraceutical purposes: Cultivation aspects. Fermentation. 4:46

125.

Sánchez-Zurano A, Lafarga T, Morales-Amaral MM, Gómez-Serrano C, Fernández-Sevilla JM, Acién-Fernández FG, Molina-Grima E. 2021; Wastewater treatment using Scenedesmus almeriensis: Effect of operational conditions on the composition of the microalgae-bacteria consortia. J Appl Phycol. 33:3885-3897

126.

Sanjari S, Sarhadi H, Shahdadi F. 2018; Investigating the effect of Spirulina platensis microalgae on textural and sensory properties of baguette bread. J Nutr Food Secur. 3:218-225

127.

Sathasivam R, Radhakrishnan R, Hashem A, Abd_Allah EF. 2019; Microalgae metabolites: A rich source for food and medicine. Saudi J Biol Sci. 26:709-722

128.

Šefcová MA, Santacruz F, Larrea-Álvarez CM, Vinueza-Burgos C, Ortega-Paredes D, Molina-Cuasapaz G, Rodríguez J, Calero-Cáceres W, Revajová V, Fernández-Moreira E. 2021; Administration of dietary microalgae ameliorates intestinal parameters, improves body weight, and reduces thawing loss of fillets in broiler chickens: A pilot study. Animals. 11:3601

129.

Seghiri R, Kharbach M, Essamri A. 2019; Functional composition, nutritional properties, and biological activities of Moroccan Spirulina microalga. J Food Qual. 2019:3707219

130.

Shaikh R, Rizvi A, Pandit S, Desai N, Patil R. 2022; Microalgae: Classification, bioactives, medicinal properties, industrial applications, and future prospectives. In An integration of phycoremediation processes in wastewater treatment. In: Shah MP, Rodriguez-Couto S, Vargas-De-La-Cruz C, Biswas JK, editors.(ed)Elsevier. Amsterdam, The Netherlands: pp p. 451-486

131.

Shantkriti S, Pradeep M, Unish KK, Das V, Nidhin S, Gugan K, Murugan A. 2023; Bioynthesis of silver nanoparticles using Dunaliella salina and its antibacterial applications. Appl Surf Sci Adv. 13:100377

132.

Sikiru AB, Arangasamy A, Alemede IC, Egena SSA, Bhatta R. 2019; Dietary supplementation effects of Chlorella vulgaris on performances, oxidative stress status and antioxidant enzymes activities of prepubertal New Zealand white rabbits. Bull Natl Res Cent. 43:1-7

133.

Singh A, Rai A, Rai PK, Sharma NK. 2023; Biodiversity and biogeography of microalgae with food and feed potential. In Handbook of food and feed from microalgae: Production, application, regulation, and sustainability. In: Jacob-Lopes E, Queiroz MI, Maroneze MM, Zepka LQ, editors.(ed)Elsevier. Amsterdam, The Netherlands: pp p. 9-21

134.

Sriwattana S, Chokumnoyporn N, Brennan C, Prinyawiwatkul W. 2024; Chemical composition and sensory profile of Spirogyra neglecta (Hassall) Kützing. Int J Food Sci Technol. 59:9336-9344

135.

Stirk WA, van Staden J. 2022; Bioprospecting for bioactive compounds in microalgae: Antimicrobial compounds. Biotechnol Adv. 59:107977

136.

Sun T, Kalia S, Wyman BM, Ou KJ, Lei XG. 2024; Impacts of feeding three strains of microalgae alone or in combination on growth performance, protein metabolism, and meat quality of broiler chickens. Algal Res. 83:103691

137.

Surendhiran D, Li C, Cui H, Lin L. 2021; Marine algae as efficacious bioresources housing antimicrobial compounds for preserving foods: A review. Int J Food Microbiol. 358:109416

138.

Talero E, García-Mauriño S, Ávila-Román J, Rodríguez-Luna A, Alcaide A, Motilva V. 2015; Bioactive compounds isolated from microalgae in chronic inflammation and cancer. Mar Drugs. 13:6152-6209

139.

Tapia-López L, Chairez I, Guerrero-Barajas C, Fernandez-Linares LC. 2024. Effect of nitrogen source and its concentration on Scenedesmus dimorphus productivity under photoautotrophic growth conditions. Available from: https://www.authorea.com/users/726754/articles/709034-effect-of-nitrogen-source-and-its-concentration-on-scenedesmus-dimorphus-productivity-under-photoautotrophic-growth-conditionsAccessed at Sep 20, 2024
.

140.

Tolba SA, Magnuson AD, Sun T, Lei XG. 2020; Dietary supplemental microalgal astaxanthin modulates molecular profiles of stress, inflammation, and lipid metabolism in broiler chickens and laying hens under high ambient temperatures. Poult Sci. 99:4853-4860

141.

Uribe-Wandurraga ZN, Igual M, García-Segovia P, Martínez-Monzó J. 2019; Effect of microalgae addition on mineral content, colour and mechanical properties of breadsticks. Food Funct. 10:4685-4692

142.

Varzaru I, Untea AE, Panaite TD, Turcu R, Saracila M, Vlaicu PA, Oancea AG. 2024; Chlorella vulgaris as a nutraceutical source for broilers: Improving meat quality and storage oxidative status. Foods. 13:2373

143.

Vlaicu PA, Untea AE, Oancea AG. 2024; Sustainable poultry feeding strategies for achieving zero hunger and enhancing food quality. Agriculture. 14:1811

144.

Vlaicu PA, Untea AE, Varzaru I, Saracila M, Oancea AG. 2023; Designing nutrition for health: Incorporating dietary by-products into poultry feeds to create functional foods with insights into health benefits, risks, bioactive compounds, food component functionality and safety regulations. Foods. 12:4001

145.

Wang Y, Tibbetts SM, McGinn PJ. 2021; Microalgae as sources of high-quality protein for human food and protein supplements. Foods. 10:3002

146.

Yan L, Kim IH. 2013; Effects of dietary ω-3 fatty acid-enriched microalgae supplementation on growth performance, blood profiles, meat quality, and fatty acid composition of meat in broilers. J Appl Anim Res. 41:392-397

147.

Yang Y, Zhang X, Hu X, Zhao J, Chen X, Wei X, Yu X. 2022; Analysis of the differential metabolic pathway of cultured Chlorococcum humicola with hydroquinone toxic sludge extract. J Clean Prod. 370:133486

148.

Yatao X, Saeed M, Kamboh AA, Arain MA, Ahmad F, Suheryani I, Abd El-Hack ME, Alagawany M, Shah QA, Chao S. 2018; The potentially beneficial effects of supplementation with hesperidin in poultry diets. World’s Poult Sci J. 74:265-276

149.

Zanella L, Vianello F. 2020; Microalgae of the genus Nannochloropsis: Chemical composition and functional implications for human nutrition. J Funct Foods. 68:103919