Abstract
The gut microbes of fish encompass various effects on the host such as the size of the fish, their metabolism, food, feeding behavior, and immunity. The process is mediated through interaction between microbes and the gut-brain axis. In fish larvae, the microbes are introduced from the egg, surrounding water, and their first feed. However, there is species-specific variation in the colonization of microbial communities. The microbial composition of the gut varies; some dominant microbes are Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, and Fusobacteria. The various environmental, ecological, and evolutionary factors affect intestinal microbial communities and their functions. Various intrinsic factors also influence the gut microbes such as phylogeny, sexual state, life stages, trophic status, and genetics. The gut microbial community modulates the host’s physiology and the host provides nutrients to the gut microbes. The gut microbial activity depends on the composition and the diversity of gut microbes. The feeding, digestion, and metabolism of the host can be affected by gut microbes. In addition, it also influences stress response, reproduction, development, and immune response. Food and feeding alteration can change the gut microbial community. The inclusion of different proteins, lipids, probiotics, prebiotics, etc. can alter the gut microbes and enhance the health status.
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1 Introduction
Microbes are different microorganisms, present in the environment. Microbiome refers to the characteristic microbial community inhabiting a well-defined habitat with distinct physicochemical parameters (Whipps et al. 1988). Microbes are ubiquitous and present across all life-sustaining habitats on Earth; the differences exist in the varied environment which carries different microbial communities. Microbes are not only present in these external environments, but they are also found to be associated with many eukaryotic hosts (Sullam et al. 2012). The impact of microbial communities on the health of various types of the host such as plants, fish, and terrestrial animals including humans has gained wide attention nowadays (Brugman et al. 2018). The microbiota can offer various benefits to the host by supplementing adequate nutrients, inducing host immune development and metabolism, and protecting the host against invading pathogens (Brugman et al. 2018). Vertebrates’ gastrointestinal (GI) tract is a composite microbial ecosystem containing a complex and dynamic association of microorganisms, which have crucial roles in the nutrition and health of the host (Wang et al. 2018). The various environmental factors influence the microbial community composition; at the same time microbes also influence the host environment (Bletz et al. 2017).
2 Gut Microbiota
Gut microbiomes are the microbes present in the intestine. The gut microbiomes of fish encompass various effects on the host such as the overall size of fish, their metabolism, food and feeding behavior, and their immunity (Yukgehnaish et al. 2020). The gut microbes are dynamic. These microbiomes are either transient or persistent, depending on the duration they live in the gut microbiota (Prasanth et al. 2018). The persistent microbiota lives in association with the gut wall and has a symbiont relationship with the host (Zhang et al. 2016). The transient microbiota comes through external sources such as food and does not live for a longer period in the stomach (Yukgehnaish et al. 2020).
3 Origin and Sources of Gut Microbes
Various factors control the gut microbial content of an infant. In fishes, the origin of gut microbes is still in the infant stage. In humans, it has been suggested that the gut microbes might have been introduced through the birth canal, pass through the oral cavity to the placenta, or subsequently introduced through the gastrointestinal tract in infants during breastfeeding (Prince et al. 2014; Gueimonde et al. 2006). In fish larvae, the entrance of microbes occurs from the egg, the adjacent water, and their initial feed (Egerton et al. 2018). However, there is species-specific variation in the colonization of microbial communities (Egerton et al. 2018). The species-specific variation in the microbial community in the larvae represents the variation of egg glycoprotein (Larsen 2014). The variation of these microbes depends on the variation of the surrounding environment from where the microbes are being attached to the egg surface. The chorion-attached bacteria subsequently colonize the gut of the newly developed larvae (Larsen 2014). The colonization of bacteria further diversifies when the larvae take the water from the environment (Lauzon et al. 2010). The feeding habit of fish also influences their microbial diversity and changes as the larvae develop into fry, fingerling, and adults (Ringø and Birkbeck 1999; Egerton et al. 2018). It has been observed that this microbial population becomes stable within the first 50 days in various species (Larsen 2014).
4 Diversity of Gut Microbes
The variability is one of the remarkable features of GI microbiota in fishes. It is not yet fully understood the complex process involved in the regulations of these bacterial populations in the GI tract of fish. Few studies have been focused on fishes such as Rainbow trout, Common carp, Atlantic cod, Atlantic salmon, Grass carp, and Zebrafish (Wang et al. 2018). The microbial composition of the gut varies although some dominant microbes are Actinobacteria, Bacteroidetes, Firmicutes, Fusobacteria, and Proteobacteria (Eichmiller et al. 2016). The various environmental, ecological, and evolutionary factors affect intestinal microbial communities and their functions. Various intrinsic factors also influence the gut microbes such as phylogeny, sexual state, life stage, trophic status, and genetics (Egerton et al. 2018). Closely related mammals having similar diets are found to harbor similar gut microbes (Sullam et al. 2012). The diversity of gut microbes also varies between fish species and within fish species. The composition of gut bacteria in fishes can be determined by the habitat, trophic level, and possibly host phylogeny shape (Sullam et al. 2012). Various research proved that the microbial flora composition varies (Table 1) in different fish species owing to their nutrition, intestinal microenvironment, age, geography, environmental factors, stress, etc. (Verschuere et al. 2000; Skrodenyte-Arbaciauskiene et al. 2008). The variation of gut microbiota depends up on the type of fish species and environmental conditions such as developmental stage of fish, feeding regime, seasonal variation, temperature, pH, nutrients intake, captive sate, and sexual state which allows the host to perform different functions and enables the host to thrive in various conditions (Hansen and Olafsen 1999; Dhanasiri et al. 2011; Hovda et al. 2012; Miyake et al. 2015; Apajalahti 2005; Cordero et al. 2015). The most influencing factor to affect the diversity of fish is trophic status, habitat of the fish, and host ancestry (Sullam et al. 2012).
4.1 Trophic Level
The gut microbes of the fishes change with the trophic status of the fish and correlate it with the availability of natural food and their feeding behavior (Liu et al. 2016). The understanding of fish gut microbiota and their role in the digestion of food is vital (Wang et al. 2018). This will help to accelerate the digestion and health of fish for the culture of various fish species. Various studies have been done to find the gut microbial composition of fish with different feeding habits (Givens et al. 2015). It has been found that the gut microbial content of herbivores is distinct from carnivorous fish (Liu et al. 2016). The planktivorous and benthivorous showed unique microbial content for different fish species in their gut (Uchii et al. 2006). However, the bacterial diversity is found lesser in carnivores, and gradually increases in omnivores and herbivores (Wang et al. 2018). The gut microbiota varies with species belonging to the same trophic level as observed in herbivorous fishes like silver carp, bighead, and grass carp (Li et al. 2018).
The digestive tract of herbivorous fish harbors anaerobic bacteria of the phylum Firmicutes and class Clostridia (Mouchet et al. 2012). The dominance of Firmicutes in the gastrointestinal tract has been observed in many fish species (Clements et al. 2007; Miyake et al. 2015). The microbes repeatedly occur in omnivores, planktivores, and carnivores are Aeromonas, Pseudomonas, and Vibrionaceae (Egerton et al. 2018). The microbes such as Pseudomonas spp., Aeromonas, and Photobacterium spp. produce digestive enzymes such as proteases and chitinases which help in digestion (MacDonald et al. 1986; Itoi et al. 2006). However, the diversity of these microbes varies with habitat, season, feeding and sex, and age.
4.2 Genetic and Sex of the Host
The composition of microbes varies within and between species. The interspecies variation in gut microbial diversity has been observed for snout bream, bighead carp, grass carp, and silver carp (Li et al. 2018). The variation in gut microbes between sex has also been observed for stickleback (Gasterosteus aculeatus), which might be due to sex-specific microbial interaction of feed variation (Bolnick et al. 2014). But only a few studies prevail in the area and its mechanism is poorly understood.
However, among the genetics and environment, the environment has more influence on the diet composition of fishes. It has been observed that different fish species (Channel catfish and blue catfish) even in the same environmental condition may harbor the same gut microbial content (Lokesh et al. 2018).
4.3 Age of the Fish
The microbial diversity changes with the age of fish. The reason might be due to the diet variation and hormonal changes in different life stages of fish (Cantas et al. 2012). The gut microbial diversity is increased with age in catfishes (Zhang et al. 2018). In Atlantic salmon also gut microbes vary between embryo and hatchlings, and hatchings exhibited more microbial diversity (Lokesh et al. 2018).
4.4 Season
The diversity and abundance of gut microbes change with the season (Hagi et al. 2004; Sullam et al. 2012). The variation might be for a short duration or a longer period. The seasonal variation in gut microbes might have influenced due to temperature variation or due to changes in food composition in the gut (Al-Harbi and Uddin 2004). The dominant taxa vary with season (Hagi et al. 2004), and the count of total bacteria peaks during summer and autumn (Macmillan and Santucci 1990; Al-Harbi and Uddin 2004). However Neuman et al. (2016) could not find any relationship between season and change in gut microbial diversity.
4.5 Habitat
The change in habitat affects the gut microbial content. The salinity of water and temperature influence the microbial community. In black molly dominant microbes vary as the salinity increases, whereas in rainbow trout temperature changes the dominant microbes (Schmidt et al. 2015; Huyben et al. 2018). It has been observed that the microbial diversity varies between freshwater and marine habitat fishes (Vatsos 2016). Vibrio is the common microbes occurring in marine habitat fishes whereas in the freshwater fishes Aeromonas and Pseudomonas dominate (Vatsos 2016).
Various pollutants such as pesticides and heavy metals influence the gut microbial composition. In common carp and zebrafish, it has been observed that polystyrene microparticles and waterborne copper influence the microbes associated with the immunity (Meng et al. 2018; Jin et al. 2018).
In the captive state also, the gut microbes depend on many factors such as food ingredients, environment, and social behavior (Egerton et al. 2018). The altered gut microbiota in captive breeding has been reported in many freshwater and marine fish species (Bucio et al. 2006; Nelson et al. 2013). Under captive management, various factors such as stocking density, stress, feed, and use of antibiotics (Verschuere et al. 2000; Navarrete et al. 2008; Clements et al. 2014) can alter the gut microbiota. In the zebrafish model, it has been shown that there are changes in gut microbiota in captive and lab-reared fish; however, some microbes remained the same depending on their historical correlation (Roeselers et al. 2011). Various others also reported that although there are habitat-specific changes, there always exists some core microbiota (Roeselers et al. 2011).
5 Physiological Roles of Gut Microbiota
The gut microbial community modulates the host’s physiology, and the host provides nutrients for the gut microbes (Rosenbaum et al. 2015). However, the gut microbial activity depends on the composition and the diversity of gut microbes (Vigneri 2014). The host physiology which can be affected by gut microbes is feeding, digestion, and metabolism; it also influences stress response, reproduction, growth, and immunity (Butt and Volkoff 2019).
5.1 Influence of Microbiota on Feeding and Metabolism
The gut microbes have a major role in the regulation of feeding, digestive process, and metabolism (Duca et al. 2012). In fishes, limited studies have been conducted to identify the effect of microbes on feeding and metabolism (Butt and Volkoff 2019). These microbes secrete short-chain fatty acid, indoles and butyrate, etc. in the form of metabolites and affect digestion and metabolism (Butt and Volkoff 2019). These microbiotas also influence the gut neurotransmitter such as serotonin, dopamine, etc., and affect the function of the gut such as motility, release of enzyme, and feeding behavior (Yano et al. 2015; Strandwitz 2018). The gut neurotransmitter also influences the microbes and modifies the discharge of cytokines (Mittal et al. 2017).
Some of the metabolites regulate the cells of the intestine and regulate their uptake, absorption, etc., and thus affect various metabolism such as adipogenesis (Bäckhed et al. 2004). The gut microbial release also modulates the secretion of gut enzymes and thus gut motility (Cani and Knauf 2016). The released microbial compounds may also circulate to reach the brain or may regulate the release of appetite-regulating peptides which may stimulate the release of central neuropeptides (Cussotto et al. 2018).
In fish also some studies have shown the influence of gut microbiota on metabolism. The microbial community can alter the metabolism pathway of carbohydrate, fat, and protein changes in grass carp (Ni et al. 2013). In zebrafish also it has been observed that change in gut microbes changes the lipid metabolism (Semova et al. 2012).
5.2 Effect of Gut Microbial Activity on Stress Response
Fishes may get stressed due to many factors such as poor water quality, lack of oxygen, temperature, and overcrowding. The stress affects the microbial community composition and changes the gut mucus and adversely affects the nutrient absorption and immunity of the host (Cantas et al. 2012). This may decrease the feeding rate and increase the chances of pathogen infection (Sekirov and Finlay 2009) as observed in goldfish and chinook salmon (Volkoff and Peter 2004; Bernier 2010). The microbes influence the hypothalamic-pituitary-adrenal (HPA) axis which is subjected to hormone control behavioral response such as feeding (Sudo 2014).
5.3 Effect of Gut Microbial Activity on Reproduction
The exact mechanism of gut microbes on reproduction is not clear. Some studies have shown that gut microbes help in gonadal development and reproduction (Butt and Volkoff 2019). In larval fish, the supplementation of probiotics improves their development and gonadal maturation as observed in zebrafish (Avella et al. 2012; Carnevali et al. 2013). In adult zebrafish and goldfish, the probiotic microbes improved gonadosomatic indexes (GSI), produced more eggs, higher reproductive gene expression, and higher reproductive success (Ghosh et al. 2007; Carnevali et al. 2013).
5.4 Effect of Gut Microbial Activity on Development
The gut microbes vary with the developmental stages. It has been found that as the fish grows their microbial diversity increases in grass carp (Wang et al. 2015). In Zebrafish the lack of microbes impaired the development of the gastrointestinal tract and the reversal of microbes may resume the function (Lescak and Milligan-Myhre 2017). The microbes may also influence neuronal development and affect the movement and feeding and ultimately the development of fish (Phelps et al. 2017).
5.5 Effect of Gut Microbial Activity on Immunity
The gut microbes play a critical role in developing the immune response of the host fish. The pathogens are defended by the intestinal microbes in host fishes (Kim et al. 2017). These pathogens could not interrupt the gut barrier and could not hamper the brain and intestine function (Ribet and Cossart 2015). The microbes present in the gut shows a competitive behavior for space with the pathogen, and they also secrete the antimicrobial peptides to disrupt the pathogen (Kim et al. 2017). In rainbow trout, it has been observed that supplementation of beneficial microbes enhances the immunity of the host (Adel et al. 2017).
6 Adaptive Strategy for Climatic Variability
The gut microbiota is allied with the health condition of fish. These microbes can be manipulated to enhance the health status of fish. Food and feeding alteration can change the gut microbial community. The inclusion of different proteins, lipids, probiotics, and prebiotics can alter the microbes of the gut and enhance health status (Egerton et al. 2018). The variation in diet and gut microbiota has been reported by various authors (Delcroix et al. 2015; Zarkasi et al. 2016), and it could be helpful as an adaptive strategy for climatic variations.
6.1 Protein
Protein acts as a source of energy in food. At the same time, the inclusion of different protein diets can also alter the gut microbiota. The type of protein and its quantity can affect the gut microbial structure (Desai et al. 2012; Geurden et al. 2014; Zarkasi et al. 2016). Peptides and glycopeptides produced after protein hydrolysis can make changes in the gut diversity (Swiatecka et al. 2012), and the supply of direct protein hydrolysates can act as a substrate for microbes and enhance their growth (Delcroix et al. 2015). The protein hydrolysate also helps to combat pathogenic bacteria, certain peptides act as antimicrobials whereas some amino acids regulate the immune pathway and synthesis of antibodies (Kiron 2012; Sila et al. 2014; Egerton et al. 2018). Thus they assist to improve the health status of fish.
6.2 Lipids
Lipid is also the main energy basis in fish. It has been found that increasing the lipid content enhances the gut microbial diversity (Lesel et al. 1989). Variation of lipid diet alters the microbial diversity in arctic char (Ringø et al. 2002). It has been shown that change of fish oil to plant-based oil improves the gut microbial community and immunity of fish against pathogens (Lødemel et al. 2001; Ringø et al. 2002). Various microbes isolated from the gut of fishes and invertebrates such as Shewanella sp. and Vibrio sp. produce polyunsaturated fatty acids (Monroig et al. 2013). These microbes can act as a potential probiotic (Egerton et al. 2018).
6.3 Probiotics
Probiotics are live microorganisms that supply health benefits to the host. These microorganisms are used as a substitute for antibiotics in aquaculture (Abelli et al. 2009). Among microorganisms, the gram-negative bacteria, gram-positive bacteria, bacteriophages, and yeasts could be used as probiotics (Akhter et al. 2015). Bacillus and Lactobacillus are the most recurrently used probiotics in aquaculture (Merrifield and Carnevali 2014). These microbes help to increase the growth rate and modulate the immune reaction of the host (Lobo et al. 2014; Cordero et al. 2015). In the aquaculture sector, these probiotics help to improve the health and nutritional status and reduce the cost (El-Haroun et al. 2006). However it is difficult to process, store, and feed the probiotics in aquaculture (Merrifield et al. 2010).
6.4 Prebiotic
Prebiotics are the substrates used to confer a health benefit in host fishes in a selective mode (Cremon et al. 2018). The commonly used prebiotics are fructooligosaccharides, mannan-oligosaccharides, inulin, and trans-galactooligosaccharides (Ringø et al. 2016). The prebiotic also helps to improve the growth, feed conversion, nutrient uptake, and immunity of fish (Bongers and van den Heuvel 2003; Torrecillas et al. 2007; Adel et al. 2016). However, the success of prebiotic administration depends on the age of the fish, species of fish culture condition, and dose of prebiotics (Torrecillas et al. 2014).
7 Next-Generation Sequencing Study of Gut Microbes
A detailed understanding between intestinal microbiota and their host fish can depict the function and dysfunction of the host organism. Conventional culture-dependent studies on fish intestinal microbiota were conducted over the last decades (Cahill 1990). However, these microbiotas only indicate <0.1% of the total microbial community in the intestine of host fishes with low cultivability (Romero and Navarrete 2006; Navarrete et al. 2009; Zhou et al. 2014; Ghanbari et al. 2015). With the advancement in DNA sequencing and bioinformatics, extensive molecular ecology-based methods on the 16S and 23S rRNA genes have become more frequently used recently.
The next-generation sequencing (NGS) technology based on the 16S and 23S rRNA and the development of various bioinformatics software has advanced the knowledge of these microbial taxa. More efficient and budget-friendly approaches to NGS technologies have gained wide attention for studying the high dense gut microbiota composition and its genetic potential (Ghanbari et al. 2015). The emerging rapid and reliable NGS techniques can enrich the knowledge of the fish gut microbial community with promising results.
8 Conclusion
Fish gut microbes affect the physiology, immunity, and growth of fish. The gut microbial composition of fish varies in different fish species and within fish species differs in different life stages. The various intrinsic and extrinsic factors also influence the gut microbes and their activity. Fish gut microbial composition differed depending on species, sex, habitat, and feeding behavior. The gut microbial manipulation through prebiotics has the potential to promote the growth and health condition of fish.
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Kumari, K., Nair, S.M. (2022). Gut Microbes and Its Physiological Role in Fish: Adaptive Strategies for Climatic Variability. In: Sinha, A., Kumar, S., Kumari, K. (eds) Outlook of Climate Change and Fish Nutrition. Springer, Singapore. https://doi.org/10.1007/978-981-19-5500-6_9
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