Gut Microbiota and Probiotics on Metabolism in Fish,Shrimp: History
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Einar Ringø
,
Ramasamy Harikrishnan
,
Mehdi Soltani
,
Koushik Ghosh

Bacteria colonizing the gastrointestinal (GI) tract microbiota in fish and shellfish consists of allochthonous- and autochthonous bacteria. The GI tract is colonized by numerous bacteria, which stimulate metabolic functions, GI development, improve digestion, enhance the immune response, and protect against exogenous bacteria and diseases, the development of metabolic syndrome, underpin host metabolic plasticity, and vitamin synthesis and affect host health. The gut immune system involves three important defense mechanisms, (i) gut barriers, (ii) innate immunity, and (iii) acquired or adaptive immunity, which work together to improve disease resistance.

  • gut microbiota
  • probiotic administrations
  • lipid-, carbohydrate- and protein metabolism

1. Gut Microbiota and Lipid Metabolism

Two recent studies revealed that zebrafish (Danio rerio) intestine colonized by Firmicutes enhanced lipid bioavailability in the gut and liver [1][2]. Grass carp (Ctenopharyngodon idella) fed a ryegrass diet revealed that lipid metabolism was significantly improved by modulation in the gut microbiota [3], and it was proposed that the hypothesis that the metabolic role of the gut microbiota in carp was affected by dietary manipulation. Sheng et al. [4] revealed that zebrafish with intact microbiota improved the accumulation of lipids in the gut, and enhanced expression of cox15, ppary, and slc2a1a, genes related to lipid metabolism vs. that of germ-free fish. Hao et al. [5] revealed a rapid modulation of the hindgut microbiota of grass carp fed fish meal (FM) and Sudan grass (Sorghum sudanense) within 11 days. However, genes associated with lipid transport and metabolism were not significantly changed by the dietary shift.
α-lipoic acid (α-LA) is an important antioxidant in the detoxification of oxygen species [6]. In a study using genetically improved farmed tilapia fed a high-saturated-fat diet (HFD), it was displayed that the adipose triglyceride gene was up-regulated in fish fed diet supplemented with 2.400 mg kg−1 α-LA, while diacylglycerol acyltransferase 2 gene was down-regulated [7]. In addition, a significant up-regulation of the fatty acid-binding protein gene in the liver by α-LA feeding was displayed. As modulation of the gut microbiota by α-LA feeding was not investigated herein, one can speculate because, as in mice, α-LA and a high-fat diet modulated the gut microbiota [8].
In their study using yellowtail kingfish (Seriola lalandi), Ramirez and Romero [9] revealed a notable difference in the gut microbiota of wild and aquaculture-raised fish, as phylum Firmicutes was abundant in cultured fish in contrast to Pseudomonadales, which dominated in wild fish. Furthermore, lipid metabolism, biosynthesis of fatty acids, glycerolipid, glycerophospholipid, secondary bile acid, and sphingolipid were affected. Similar results on lipid metabolism were reported by Salas-Leiva et al. [10], analyzing the structure and metabolic contribution of gut microbiota in longfin yellowtail (Seriola rivoliana) juveniles.
Yildirimer and Brown [11] revealed significant enrichment of fatty acids and lipid metabolism genes in the allochthonous hindgut microbiota of Western Cascade rainbow trout compared to that of Eastern Cascade fish, even though a more diverse microbial community was revealed in Eastern Cascade fish.
Arias-Jayo et al. [12] revealed that in zebrafish fed the HFD, the dominant pathways involved were in AA metabolism in contrast to fish fed a high-saturated-fat DHA-enriched diet, where the pathways involved in lipid metabolism were prominent.
Meng et al. [13] revealed that waterborne copper exposure modulated the allochthonous microbiota and lipid metabolism in common carp (Cyprinus carpio) as intestinal Roseburia was positively associated with lipogenic enzymes, total protein, and triglycerides but negatively associated with lipolysis enzymes.

3. Gut Microbiota and Carbohydrate Metabolism

As the metabolism of carbohydrates is dependent on their source and the inclusion level of carbohydrates in the diet [14], it is important to know whether the gut microbiota can influence carbohydrate metabolism, related to the capacity of fish to utilize dietary carbohydrates as an essential supplement.
As FM and fish oil (FO) are important supplements, with increasing costs and shortages, the utilization of alternatives is becoming increasingly important, and plant feedstuffs are the most sustainable alternatives. When discussing the use of plant material, it is important to keep in mind that fish species consuming plant material (herbivores and omnivores) reveal greater diversity and abundance of intestinal bacteria than carnivores. The nutritive value of plant feedstuff is limited by a high content of non-starch polysaccharides (NSP), which cannot be utilized by fish, but low dietary inclusion levels of NSP may increase the abundance of bacteria displaying the ability to mobilize or inactivate NSP. For example, marine bacilli isolated from European sea bass (Dicentrarchus labrax) intestines were capable of hydrolyzing NSP [15], and 43 out of 160 isolates revealed high or broad carbohydrolytic capacity. Nine spore-forming isolates were efficient by metabolizing, i.e., xylose, galactose, arabinose, or mannose.
In humans, a clear context between gut microbiota and glucose metabolism disorders is revealed [16]. However, as this topic is less investigated in fish and shellfish, it merits investigation.
Wu et al. [17] revealed that intestinal microbes of Nile tilapia were positively correlated with most intestinal metabolites, including carbohydrate metabolism. Herein, Cetobacterium, a bacterial genus producing vitamin B12 and enhancing carbohydrate metabolism, was reported.
Juvenile rainbow trout fed either an experimental diet of hyperglucidic (40% gelatinized starch + 20% glucose) and hypoproteic (20%) diet or a high-protein (60%) glucose-free diet (control) revealed a rapid increase in gene expressions of glycolytic enzymes in juveniles fed the experimental diet relative to control diet, while genes involved in gluconeogenesis and AA catabolism were reduced [18]. Muscles from juveniles fed the hypoproteic diet displayed a down-regulation of glycolysis and glucose transport markers, as well as higher plasma glucose. Evaluation of the intestinal microbiota of yellowtail kingfish, wild and aquaculture, showed that the metabolism of carbohydrates, vitamins, and AA exhibited a difference in microbiota depending on the host origin [9]. A recent study revealed that the intestinal microbiota of longfin yellowtail juveniles, mainly dominated by Proteobacteria, Firmicutes, Bacteroides, Cyanobacteria, and Actinobacteria, exhibited a contribution to carbohydrate metabolism and AA metabolism [10].

4. Gut Microbiota and Protein and Amino Acid Metabolism

Dietary protein modulates AA utilization by gut microorganisms, and this has impacts on gut health [19]. For example, threonine is utilized by the gut for the synthesis of mucin and the maintenance of gut barrier integrity [20].
Gut microbiota either consume the AA synthesis from diet or AA building blocks of proteins in the host or metabolize nutrients via fermentation or conversion to form several metabolite compounds, including nitric oxide, ammonia, polyamines, hydrogen sulfide (H2S), indolic, and phenolic in both the proximal and distal intestine [19][21].
The GI tract microbiota can de novo synthesize some essential amino acids that contribute to the modification of AA homeostasis in the body [22]. At the same time, large amounts of AA and proteins undergo extensive metabolism by the intestinal bacteria or epithelial cells [22][23][24]. Digestive enzymes are formed, and nitrogen, immunoglobulins, urea, and mucins SI lumen, is further degraded, utilized, and metabolized by the intestinal microbiota.
The proteins are hydrolyzed into peptides and AAs by extracellular enzymes secreted by gut bacteria that enter the microbial cells [25]. AAs and peptide biomolecules can meet different fates [26]. For example, AAs catabolism is transamination or deamination formed by decarboxylases, and deaminases enzymes are involved in AAs metabolism to form biogenic/aromatic AAs/amines by decarboxylation through fission, deamination, decarboxylation, oxidation, and reduction or both (redox) to produce a variety of structurally related indoles and phenols [26].

5. Probiotics and Metabolism

Increasing evidence during the last decade confirmed the crucial roles of probiotics (beneficial gut microbes) in host health [27]. Numerous metabolic functions could be under close regulation of probiotic organisms. Falcinelli et al. stated that “probiotics can be used to positively alter gut microbiota, and their ability to improve metabolism” [28]. The majority of the studies dealing with probiotics and metabolism have focused on either nutrient metabolism (lipid and glucose) [1][29] or metabolites linked with stress and immunity [30]. Nowadays, zebrafish have increasingly been used as a platform for developmental as well as biomedical research on disease modeling [31]. Consequently, the zebrafish model has gained acceptance for validating the beneficial functions of potential probiotics [32].
As evidenced, probiotics administration could be strongly allied to lowering cholesterol levels in vertebrate hosts [28][33]. In a previous report, Lye et al. [34] suggested five mechanisms by which probiotics may affect lipid metabolism: (1) assimilation of cholesterol during growth, (2) binding of cholesterol to cellular surface, (3) disruption of cholesterol micelle, (4) deconjugation of bile salt, and (5) bile salt hydrolysis activity. In a review devoted to probiotic products containing mainly live lactic acid bacteria (LAB), Cho and Kim revealed decreased total cholesterol and LDL cholesterol, but no significant effect on HDL cholesterol and triglycerides was reported [35]. In zebrafish larvae, administration of Lactobacillus rhamnosus IMC 501 downregulated the transcriptions of genes involved in cholesterol (hnf4α and npc1l1) and triglyceride (fit2 and mgll) metabolism that decreased cholesterol- and triglyceride content along with increased fatty acid levels [36]. Further, adult zebrafish exposed to varying lipid levels revealed that high dietary lipid reduced the gut microbiota diversity, which affected the transcription of genes involved in appetite control, while supplementation of Lb. rhamnosus resulted in decreased total body cholesterol [37]. In adult zebrafish, administration of Lb. rhamnosus alleviated per-fluoro-butane-sulfonate (PFBS) induced gut microbial dysbiosis and lipid metabolism disorders [38]. In a follow-up study, it was noted that antagonistic interaction between PFBS and Lb. rhamnosus on glucose metabolism. PFBS alone induced elevated blood glucose levels in male zebrafish; however, probiotic supplementation led to increased insulin levels that reduced glucose accumulation and enhanced ATP production [27]. In addition, oral administration of Lb. rhamnosus on Type 2 diabetes mellitus (T2DM) was investigated in T2DM-induced adult male zebrafish. The results revealed that probiotic administration decreased the blood glucose level by decreasing pro-inflammatory cytokines responsible for signaling in T2DM [39].
In zebrafish, administration of Chromobacterium aquaticum for 8 weeks enhanced growth and metabolism, as a significant increase in expression of glucokinase, hexokinase, glucose-6-phosphatase, and pyruvate kinase and growth hormone receptor and insulin-like growth factor-1 were noticed [32]. Furthermore, C. aquaticum supplementation modulated innate immunity-related genes (IL-1β, IL-6, TNF-α, IL-10, IL-21, NF-κb, lysozyme, and complement C3b) and improved survivability in zebrafish challenged against Aeromonas hydrophila and Streptococcus iniae. Feeding xylanase-expressing Bacillus amyloliquefaciens R8 to zebrafish improved hepatic glucose, lipid metabolism, and reduced oxidative stress and immunity, and enhanced resistance against A. hydrophila and S. agalactiae [30]. Herein, increased expressions of glycolysis-related genes (e.g., hexokinase, glucokinase, glucose-6-phosphatase, and pyruvate kinase) and elevated levels of 3-hydroxyacyl-CoA dehydrogenase and citrate synthase (associated with β-oxidation and mitochondrial integrity) activities were also recorded. Further, decreased expressions of oxidative stress-related genes (SOD, Gpx, NOS2, and Hsp70) and an apoptotic gene (tp53), along with increased expression of an anti-apoptotic gene (bcl-2) and innate immunity-related genes (IL-1β, IL-6, IL-21, TNF-α, and TLR-1, -3, -4) were also noticed in probiotics-fed zebrafish suggesting the probiotic potential of B. amyloliquefaciens R8 [30]. Zebrafish-fed diets supplemented with transgenic phytase-expressing probiotic Bacillus subtilis revealed significant improvement in gene expression for appetite, peptide transport, somatic growth, and bone metabolism [40]. The likely mechanisms through which dietary supplementation of probiotics can exert favorable effects on glucose homeostasis and anti-lipidemic impacts could be related to increasing the short-chain fatty acid (SCFA) levels and metabolites with antimicrobial, anti-inflammatory, and immunomodulatory properties (e.g., bacteriocins, vitamins K and B2) [28][33][41]. Probiotics could also be linked to improved growth by increasing lipid catabolism through β-oxidation that promotes intestinal absorption of fatty acids metabolites [42]. Apart from zebrafish, probiotic efficiency linked with metabolic function has also been illustrated with other teleosts and shrimps. Olive flounder (Paralichthys olivaceus) fed Bacillus clausii displayed higher growth and feed efficiency vs. fish-fed control diets [43]. Oral administration of Shewanella putrefaciens (viable/non-viable) revealed improved growth, metabolism, immune response, and disease resistance in gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis) [44]. Lyophilized cells of S. putrefaciens significantly increased linolenic acid (C18:3 n-3) and linoleic acid (18:2 n-6) in the liver in juvenile Senegalese sole [45]. Short-term (30 d) exposure to Enterococcus faecalis FC11682 also increased both linolenic acid and linoleic acid levels in Malaysian mahseer (Tor tambroides) post larvae [46]. Linolenic acid serves as a precursor for eicosapentaenoic acid (20:5 n-3) and docosahexaenoic acid (22:6 n-3), while linoleic acid for arachidonic acid (20:4 n-6) as a precursor for eicosanoids, which are integral for cellular and metabolic activities including membrane integrity, gene regulation and immune response [46][47]. A study using Senegalese sole larvae demonstrated that S. putrefaciens administration induced changes in the expression of carboxypeptidase A1, trypsinogen, cathepsin Z, and proteasome 26S non-ATPase subunit 3 involved in digestion and metabolic functions [48].

This entry is adapted from the peer-reviewed paper 10.3390/ani12213016

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