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Soy protein is the major source of protein as fishmeal replacement in fish feed because of its worldwide availability and low price. However, the presence of high carbohydrate content along with saponins, lectins, and phytates can have a negative impact on fish gut health. Based on the literature and our lab studies, dietary soybean meal can cause a dose-dependent type of distal intestine inflammation called enteritis in commercial fish species including salmonids. This leads to reduced absorptive capacity, increased mucus secretion, hyperpermeability, and leucocyte infiltration in the lamina propria and submucosa, also inducing the pro-inflammatory cytokine genes expression, including Il-1β, Il-8, and Tnf-α. In addition, dietary soy may alter the composition and population of the gut microbiota via providing nutrients and energy that preferentially support the growth of some gut bacteria. This chapter summarizes the current knowledge of the effects of soy protein on the enteritis and gut microbiota.
Department of Animal and Veterinary Science, Aquaculture Research Institute, University of Idaho, USA
Hagerman Fish Culture Experiment Station, University of Idaho, USA
Md. Sakhawat Hossain
Hagerman Fish Culture Experiment Station, University of Idaho, USA
Department of Aquaculture, Faculty of Fisheries, Sylhet Agricultural University, Bangladesh
Janice A. Ragaza
Department of Biology, Ateneo de Manila University, Philippines
Marina Rubio Benito
Department of Animal and Veterinary Science, Aquaculture Research Institute, University of Idaho, USA
Hagerman Fish Culture Experiment Station, University of Idaho, USA
*Address all correspondence to: vikaskumar@uidaho.edu
1. Introduction
Soybean meal (SBM) is one of the most commonly used alternative plant-based ingredients to replace marine derived fishmeal (FM) in aquafeed. Relatively, high protein content and favorable amino acid profile of SBM approaches the nutritional requirement of many cultured species [1, 2, 3, 4]. In carnivorous fish species almost 20–40% fishmeal protein can be replaced by SBM protein without compromising growth, feed utilization performances, and gut health [5]. It is also well documented that high dietary soy protein inclusion resulted in lower feed intake, reduced weight gain, morphological changes of distal intestinal epithelium, and abnormal health condition of fish [6, 7, 8, 9, 10, 11, 12]. The challenges behind the high inclusion of soy protein in aquafeed includes the limiting amino acids methionine, presence of high carbohydrate level which negatively influences mainly carnivorous species, and the presence of different antinutritional factors (ANFs) [1, 2, 3]. To overcome the challenges, several techniques have been attempted viz. using different processing techniques (heat and enzymatic treatment, bioprocessing, fermentation, etc.) to improve the soy ingredient profiles like increased protein levels, decreased levels of ANFs, and enhanced digestibility [13, 14, 15]. For balancing amino acids profile, a balance mixture of soy protein with other plant ingredients protein and crystalline amino acids supplementation were also practiced. However, SBM of standard quality is used in carnivorous fish diets only at relatively low levels due to its negative effects on gut health in several fish species [16]. Different soy protein sources have been found to modulate many aspects of gastrointestinal tract (GIT) health within fish species, including the histological composition, immune status, and the overall intestinal microbiota [17, 18, 19, 20, 21, 22, 23]. Intestinal morphology, gut-associated immunity, and microbial community are closely interacting with each other. The present chapter addresses the potential impacts of different soy protein inclusion in aquafeed on gut health condition of fish with special emphasis on gut morphology, soybean meal-induced enteritis (SBMIE), gut-associated immunity, and gut microbiota.
2. Effect of soybean meal inclusion in aquafeed to induced enteritis (SBMIE) in fish
When studying enteritis in fish, it is important to consider all cell types involved in a correct function of the gastrointestinal tract (GIT). Like mammals, fish gut is critical for nutrient digestion and absorption, immunity, and interaction with the environment [24, 25, 26]. In fish, a simpler division of the GIT is described as compared to mammals: two different segments of the gut are distinguished: proximal or anterior intestine and distal or posterior intestine (Figure 1a,b). Of these, distal intestine is where most of the nutrient absorption occurs and is the object of study of SBMIE in fish [28, 29, 30, 31, 32, 33].
Figure 1.
(a) On top: Different section-planes through the digestive tract of the rainbow trout. Below: Sections through segment 1, 2, and 3 consisting of Liver (L), stomach (S), foregut (F) with pyloric appendices (P), hind gut/rectum (E) (Source: [27]). (b) (A) rainbow trout stomach showing well-developed gastric glands (G), submucosa (S), and the tunica muscularis (M). (B) Higher magnification of branched tubular gastric glands. Asterisk (*) represents Shape and cellular morphology of mucous and (+) indicates pepsin and hydrochloric acid producing cell-type (oxyntopeptidic cells) (Source: [27]).
The word enteritis refers to an inflammatory process happening in the gut, which can be caused by a diverse range of factors. The symptoms that define the condition are a shortening of the mucosal folds, a loss of the normal supranuclear vacuolization of the absorptive cells in the intestinal epithelium, a widening of the central stroma within the mucosal folding, with increased amounts of connective tissue, a profound infiltration of inflammatory cells in the lamina propria [4, 6, 19, 34, 35, 36, 37], an increased presence of IgM [38], an increased amount of goblet cells in the epithelium, as well as a decreased height of the microvilli together with increased microvillar vesicle formation [36]. Baeverfjord and Krogdahl [6] also described this condition as “a non-infectious sub-acute inflammation of the distal intestine.” Typically, FM replacement by SBM in fish diets is between 20 and 40% at which signs of enteritis are detected in a large variety of both marine and freshwater species including omnivores and carnivores [39]. A reduction on feed intake and consequent decrease in weight gain is the first indicator that a given diet is exerting a negative effect.
There are several factors affecting the occurrence of SBMIE such as the inclusion levels, varieties, origins, and processing techniques of the different soybean products along with species variation and husbandry conditions (temperature, salinity, etc.). Nordrum et al. [40] who investigated the effect of salinity on the development of enteritis in salmonids. Urán [41] reported that with the increasing water temperature, the metabolic rate of Atlantic salmon increased which help to increase the severity of enteritis. Regarding the species variation effects on SBMIE, Nordrum et al. [40] also found that the effects of SBM on the intestinal morphology of rainbow trout were of less magnitude than for salmon. Similarly, Booman et al. [42] reported that soybean meal induced enteritis in Atlantic salmon (Salmo salar) and Chinook salmon (Oncorhynchus tshawytscha) but not in pink salmon (O. gorbuscha).
To understand the mechanism of intestinal inflammation or enteritis, it is important to also understand the elements involved at the cellular level. Enterocytes are cuboidal shaped epithelial cells that are distinct on their apical surface than on their basal surface. The apical surface faces the intestinal lumen and shows the characteristic folding of intestinal cells, called microvilli. The basal side is connected to vasculature where absorbed nutrients are released. Nutrients can undergo transcellular transport on the apical and basolateral membranes of the cell; this can happen by diffusion or by active transport through transmembrane transporters like the glucose/Na+ cotransport system, or other amino acid transporters like glutamine transporter, and also through pumps and channels. Paracellular transport occurs in between epithelial cells, and only small molecules and ions, solutes, and fluids can reach the blood this way. Only small nutrients can diffuse this way, as, in healthy conditions, enterocytes are held together through important tight junctions that keep the intestinal integrity [31, 32]. Intercellular exchange between enterocytes is also possible though gap junctions and desmosomes. Figure 2 showing the healthy and abnormal enterocyte condition in fish.
Figure 2.
Figure showing the healthy and abnormal enterocyte condition in fish.
Some tight junction proteins that have been studied in fish with regards to SBMIE include transmembrane proteins like occludins and claudins and intracellular components like zonula occludens-1 (ZO-1) [26, 28, 31, 32]. Another intracellular component that interacts with the tight junction complex is myosin light chain kinase (MLCK), involved in cytoskeletal contraction, smooth muscle contraction, and, therefore, tight junction regulation and paracellular permeability [26, 43, 44].
3. Morphophysiological effects at fish gut of soy protein inclusion in aquafeed
Although soy protein has widely been used in aquafeed as a cheap alternative protein source for FM; however, the presence of some ANFs in SBM restricts its level of inclusion in aquafeed. High inclusion of soybean ingredients causes several negative effects on palatability and intestinal morphology of fish. From previous researches, it is well documented that high inclusion of soybean meal (>40%) causes several intestinal morphological changes such as the reduction in mucosal folding, reduced fold height, enterocyte height, microvillus height, loss of mucosal integrity, abnormal vacuolization, and inflammatory cell infiltration (Figures 3a–c and 4a–1,a–2,b–1,b–2) in aquatic animals [5, 6, 7, 8, 36, 45, 46, 47, 48, 49]. The degree of morphological changes in the intestine depends on the inclusion level of SBM which is also correlated with the cultured fish species. Reduced fold height, enterocyte height, and microvillus height reduced the area of nutrient absorption in the intestine which finally affects the fish performances.
Figure 3.
(a) Intestinal histology (posterior, intestine, 20 X) of rainbow trout (O. mykiss) fed FM-based control diet showing normal condition of intestine (Kumar et al., unpublished data). (b) Intestinal histology (posterior, intestine, 20 X) of rainbow trout (O. mykiss) fed low SBM (10.3%)-based diet showing inflamed muscularis, leukocyte infiltration of the lamina propria leading to swelling and mucosal fold fusion (bridging). Increased prevalence of globlet cells possibly to secrete more mucous to protect the epithelium. Asterisk denotes inflammation (Kumar et al., unpublished data). (c) Intestinal histology (posterior, intestine, 20 X) of rainbow trout (O. mykiss) fed high SBM (20.7%) based diet showing villi and lamina propria highly inflamed (leading to much wider mucosal folds), muscularis inflamed, villi shortened, disorganization of epithelium, reduction in supranuclear absorptive vacuoles, mucosal fold fusion (bridging) and some structural disintegration. By far, this treatment led to the most changes (Kumar et al., unpublished data).
Figure 4.
(a-1) Cross-section of anterior intestine (X 40, HE) of Amberjack (Seriola dumerili) fed FM-based control diet showing increased fold height (hF). (a-2) Cross-section of anterior intestine (X 400, HE) of Amberjack (Seriola dumerili) fed FM-based control diet showing increased enterocyte height (hE) and microvillus height (hMV). (b-1) Cross-section of anterior intestine (X 40, HE) of Amberjack (Seriola dumerili) fed 50% FM replaced with SBM-based diet showing reduced fold height (hF). (b-2) Cross-section of anterior intestine (X 400, HE) of Amberjack (Seriola dumerili) fed 50% FM replaced with SBM-based diet. Showing reduced enterocyte height (hE) and microvillus height (hMV).
Feed nutrients must be digested for their utilization, and pancreatic digestive enzymes have essential roles for the digestion; trypsin and chymotrypsin are the main pancreatic proteases, lipase is the major pancreatic lipolytic enzyme, and amylase is known as the major pancreatic digestive enzyme for carbohydrates (Murashita et al. [50]). Inclusion of SBM that also affects the digestive enzyme secretion of different fish species is well documented. Murashita et al. [50] reported that red sea bream fed SBM showed lower content and activity of four pancreatic digestive enzymes compared to fish fed FM. Also, lower gene expression levels of the digestive enzymes in the hepatopancreas were observed in the SBM fed red sea bream compared with the FM fed fish, which is in line with the report in yellowtail; orally administrated FM increased the trypsin and lipase gene expressions in the pyloric caeca, but not in fish administrated SBM [51]. Perera and Yúfera [52] reported that early SBM feeding of S. aurata larvae significantly affects the activity of most pancreatic enzymes in a time-of-exposure dependent form. More than 10 days of SBM feeding (i.e., beyond 14 dph) delayed the normal development of S. aurata larvae digestive capacities as the activities of all trypsin, chymotrypsin, and amylase were significantly reduced. This is opposed to the typical response of juvenile and adult fish to SBM. Protease inhibitors present in SBM can partially abrogate the activity of trypsin and chymotrypsin in the proximal intestine [53], and juveniles of S. aurata [54] and other fish such as Atlantic salmon [55, 56] exhibit a rapid compensatory increase in activities of these enzymes. However, SBM-induced increase in trypsin activity in juvenile fish is more marked in the distal intestine and has been attributed to a reduced ability to reabsorb the pancreatic enzymes [11] and the upregulation of trypsin-like activity by immune cells [56]. Therefore, other plausible explanation for our observations is that these intestinal processes are not fully functional in early larvae. Conversely, lipase activity was relatively insensitive to SBM in S. aurata larvae, as reported before in postsmolt Atlantic salmon [55]. The observed decrease in pancreatic proteases may be responsible for less lipase inactivation in the digestive tract explaining the stable lipase activity.
4. Soy protein inclusion impacts on gut-associated immunity
The gastrointestinal tract carries many functions in teleost; among them, defense is possibly one of the most important functions. Gut acts as a physical barrier to pathogen entry that also contains a gut-associated lymphoid tissue (GALT). Teleost gut-associated lymphoid tissue (GALT) consists of leucocyte populations located both intraepithelially and in the lamina propria with no structural organization. The gut microbes play a critical role in the development and maturation of GALT, which in turn mediate a variety of host immune functions [49]. Recent work on the structure of GALT and other intestinal cell populations, the absorption of macromolecules from the intestinal lumen, and the production of specific mucosal antibodies strongly suggests, however, that the gut of these lower vertebrates is immunocompetent. Fish intestine, especially the posterior segment, is immunologically active and armored with various immune cell types, including B cells, macrophages, granulocytes, and T cells [57, 58]. Studies on the gut-associated immunity are important for the aquaculture industry for several reasons. First, the gut is one of the main portals of entry of pathogens. Second, farmed fish are generally fed commercial pellets, which give farmers the ability to manipulate fish health by incorporating drugs, vaccines, and different feed ingredients or additives into the feed. Third, the gut immune system of teleost’s allows microbial colonization by symbionts, and this microbial community can be regarded as a mechanism to modulate fish pathogens [59]. Many studies attempt to reveal the effects of inclusion of plant origin ingredients and different feed additives on gut-associated immunity in fish. In this current chapter, an attempt has made to discuss the effects of soy protein ingredients inclusion in aquafeed on gut-associated immunity of various fish species.
Research conducted on the modulation of gut immune response due to the inclusion of soy products in aquafeed predominantly concentrate on innate immune parameters. Several molecules involved in innate immunity are found in the intestine of different fish species, such as lysozymes in Asian sea bass (Lates calcarifer) [60] and Atlantic salmon (Salmo salar L.) [61]; complement components in grass carp (Ctenopharyngodon idella) [62], rainbow trout (Oncorhynchus mykiss) [63, 64], and Asian sea bass [65]; cytokines in Atlantic cod (Gadus morhua) [66] and rainbow trout [67]; lectins in several species (reviewed in [68]); or antimicrobial peptides (AMPs) in rainbow trout [69] and grouper (Epinephelus coioides) [70].
The immune status of a fish’s intestinal mucosa is closely associated with inflammation, which is mediated by cytokines. Cytokines, such as IL-1, IL-10, and IL-16 have a fundamental role in the regulation of inflammatory responses in fish throughout the infection process [31, 32]. Many studies have shown that IL-1 and IL-16 are increased in inflammatory bowel disease and there was a positive association between disease activity [71, 72]. While the deprivation of IL-10 evokes the development of inflammatory bowel disease, the decrease of IL-10 can aggravates local inflammation [73, 74]. Wang et al. [75] reported the increased expression levels of IL-1 and IL-16 mRNA with the SBM level in the diet, whereas the IL-10 mRNA expression level decreased with the SBM level in the diet of orange-spotted grouper (Epinephelus coioides). At the same time, infiltrate leucocytes were observed in the intestinal epithelium in grouper fed diets contained SBM. Furthermore, the degree of intestine inflammation was positively correlated with IL-1 and IL-16 mRNA expression levels but negatively correlated with expression of IL-10 mRNA. Their results suggest that SBM can cause intestinal inflammation by increasing pro-inflammatory cytokine levels and decreasing anti-inflammatory cytokine levels.
Krogdahl et al. [35] examined the effect of solvent and alcohol extracted SBM in the diets of Atlantic salmon, and their results indicated that fish fed solvent-extracted SBM showed higher mortality rate when challenged by A. salmonicida. In addition, fish fed alcohol-extracted SBM revealed increased levels of both lysozyme and IgM in the mid and distal intestinal mucosa. In Atlantic salmon, Lilleeng et al. [76] showed significantly downregulated TGF-β gene expression after on day feeding of extracted SBM (460 g kg−1), whereas reduced expression of interferon-inducible lysosomal thiol reductase (GILT) was observed followed by 3 days feeding. The authors assumed that the downregulation of TGF-β and GILT might be due to the failure to maintain mucosal integrity in the distal intestine. Sahlmann et al. [77] investigated transcriptomic profiling in Atlantic salmon feeding of SBM (200 g kg−1) containing diet for 1 week. On days 3 and 5, a prominent change in gene expression patterns was observed. Immune-related genes were upregulated during the first 5 days: GTPase IMAP family members; NF-kB-related genes; and regulators of T-cell and B-cell function. These immune genes expression profiles suggest that intestinal inflammation is induced within a week upon administration of an SBM-containing diet, which may in turn negatively influence the growth performance of salmonids.
Bruce et al. [29] evaluated processed soybean meal ingredients (defatted soybean meal, bioprocessed soybean meal [BSBM], and commercial soy protein concentrate [CSPC]) inclusion in the diets of rainbow trout on intestinal immunity. They reported no significant differences in intestinal immunoglobulin concentrations (p = 0.41) or gut leukocyte phagocytosis at day 15 samplings (p = 0.41). Intestinal lysozyme activity showed some modulation throughout the feeding trial period, with the BSBM diet producing higher levels in the long-term sample (60 day). A previous study on Atlantic salmon (Salmo salar) showed increased lysozyme activity in the intestinal mucosa due to the dietary inclusion of soybean molasses, indicating a potential inflammatory response and was potential activation of leukocytes [35]. Kim and Austin [78] also found high lysozyme activity in rainbow trout intestinal mucus samples after the administration of probiotics compounds which may be closely related to bioprocessed plant-based ingredients. Therefore, increased lysozyme levels may also be indicative of intestinal innate immunity and gut health enhancements.
The mucosal immune system in fish includes certain immunocompetent cells and factors in the intestinal mucous membrane. Of these factors, the interleukins (ILs), interferon regulatory factors (IRFs), and tumor necrosis factors (TNFs) are the main immune-relevant factors linked to inflammation in the distal intestine in fish [79]. Recently Miao et al. [80] reported the substitution effects of dietary SBM on the mucosal immune system in northern snakehead through measuring the gene expression of certain inflammatory cytokines (IL-1β, IL-8, IL-10, and IL-17F) in the distal intestine. After 63-day feeding, trial results indicated that dietary soybean meal affected the gene expression of certain factors. The up-regulated relative expression of IL-1β in the fish fed diet group containing 75% defatted fishmeal replacement with SBM was consistent with the observations in Atlantic salmon [77, 81]. However, the level of IL-1β observed in the same diet group was only 1.6-fold higher than that in FM-based control diet, while that observed in Atlantic salmon was 20-fold higher [79]. The effect of dietary soybean meal on the expression of IL-1β reflects the fish species and stages due to the different tolerance capability for soybean meal [79].
5. Effects of soy protein inclusion on gut microbiota
Healthy gut microbiota is essential to promote host health and well-being. Before the 1970s, there were some controversies regarding the existence and role of an indigenous microbiota in fish. However, it is now well established that fish and other aquatic animals have a microbiota in the GI tract (for review, see; [21, 23, 82, 83, 84, 85, 86, 87, 88, 89, 90, 91, 92]). The intestinal microbiota of fish, as is the case of mammals, is classified as autochthonous (indigenous) or allochthonous bacteria [90, 93]. The autochthonous bacteria are those able to colonize the host’s gut epithelial surface or are associated with the microvilli, while the allochthonous bacteria are incidental visitors in the GI tract and are expelled after some time without colonizing [90, 93]. Several factors affect the gut microbiota in fish including host factors, environmental factors, microbial factors, etc. However, until recently, among different influencing factors affecting the fish microbiota, water and diet (environmental factors) have been studied extensively [49]. In this section, we address the effect of dietary soybean products on intestinal bacterial community of finfish and crustaceans (Table 1).
defatted soybean meal (SBM), bioprocessed soybean meal (BSBM) and commercial soy protein concentrate (CSPC) replaced approximately 73% menhaden fishmeal and fed for 60 days
The incorporation of processed soy-based proteins alters the microbial community composition within the distal intestine. Species diversity based on abundance and evenness were lowest in the SBM group, and were significantly less than the BSBM-L (p = 0.003) and CSPC (p = 0.003) treatments
↑ autochthonous bacteria in MI and DI, allochthonous in DI → no. of genera and strains ↑ Brevibacterium, Enterococcus, yeast ↓ Marinilactobiacillus psychrotolerans, C. maltaromaticum
→ total autochthonous bacteria (proximal Aintestine; PI), total allochthonous bacteria, allochthonous community composition and total autochthonous bacteria (DI) ↑ autochthonous Enterobacteriaceae, Bacilli-like, Lactobacillaceae, Streptococcaceae in PI ↓ autochthonous Vibrionaceae in PI ↑ autochthonous Bacilli- like, Streptococcaceae in DI
↓ the diversity indices in DI, Weissella confusa in the DI, proportion of Photobacterium in MI ↑ relative abundance of Firmicutes compared with the FM group, abundance of Lactococcus lactis subsp. Lactis in MI → Photobacterium in DI
FM replaced with graded level of SBM and fed for 63 days
At the phylum level, ↓ Firmicutes abundance was the lowest in the diet group having 75% defatted fishmeal replacement with SBM, ↑In contrast with Proteobacteria, Bacteroidetes and Planctomycetes ↓At the genus level, significantly lower abundance of Lactococcus, Geobacillus, Pseudomonas, Streptococcus, Bacillus and Acinetobacter in diet group (75% defatted fishmeal replacement with SBM) ↑ but higher abundance of Cetobacterium, Planctomyces, Shewanella, Thermomonas, Rubrivivax and Carnobacterium was observed in fish fed the same diet group (75% defatted fishmeal replacement with SBM)
Effects of soy protein inclusion on gut microbiota of fish.
5.1. In salmonids
Research conducted until recently on SBM inclusion effects on gut microbiota of fish indicated that SBM modulated the intestinal microbiota toward developing an undesirable microbial community that can induce mucosal inflammation [110, 111]. Heikkinen et al. [94] reported that rainbow trout fish fed FM- and SBM-based diets for 4 weeks showed decreased number of cultivable intestinal bacteria (aerobic and anerobic). Afterward, by the 8 weeks of feeding trial, the bacterial numbers increased in the FM group, but not in the SBM group. Length heterogeneity analysis of PCR amplified 16S rDNA (LH-PCR) data also suggested a diet-related qualitative change in the intestinal microbiota of fish. The dominant identified genera were among aerobic species Aeromonas, Sphingomonas, and Chryseomonas and among the lactic acid bacteria, the genera Lactococcus and Lactobacillus. Rainbow trout fed SBM (450 g/kg) for 16 weeks showed decrease in total culturable species of Aeromonas spp., Vibrio spp., but the species Actinomycetales, Psychrobacter spp., Saccharomyces spp. were found as increased number. Total culturable aerobic levels, Micrococcus spp., were found unchanged in numbers. Mansfield et al. [96] evaluated the effect of FM and SBM (300 g/kg) on the allochthonous distal intestinal microbiota of triploid female rainbow trout by three cpn60 universal clone libraries, resulting in 1000 and 1181 sequences from FM and SBM, respectively. There were total 32 different sequences were noticed. The most frequently observed sequences were identical to Carnobacterium (piscicola) maltaromaticum and accounted for 55 and 97.2% of the clones from the FM and SBM group, respectively. Overall, fish fed FM showed highest diversity (14 different sequences) and only four different sequences observed in the SBM library. In another study, Desai et al. [97] observed that 30% SBM inclusion in rainbow trout diets led to a reduction in Proteobacteria and increase in Firmicutes. Recently, Bruce et al. [29] evaluated different processed soybean products as a replacement of fishmeal on gut microiota of rainbow trout and observed that the incorporation of processed soy-based proteins alters the microbial community composition within the distal intestine. Species diversity based on abundance and evenness were lowest in the defatted soybean meal group and were significantly less than the bioprocessed soybean meal in low concentration (p = 0.003) and commercial soy protein concentrate (p = 0.003) treatments.
In Atlantic salmon, fish fed the SBM (250 g/kg) diet had higher total number as well as a more diverse population composition of adherent bacteria in the distal intestine observed by Bakke-McKellep et al. [98]. Green et al. [100] investigated the influence of FM and soybean protein concentrate (SPC; 50 g/kg) on intestinal microbiota of Atlantic salmon. Terminal restriction fragment length polymorphism (T-RFLP) and 16S rRNA clone library analysis revealed that the SPC diet modulated the intestinal microbiome by increasing the bacterial diversity, and a Pseudomonadales was more frequently revealed species. In addition, increased Escherichia coli also observed in SPC-based diet, but it was absent in FM-based diet. In another study, Navarrete et al. [101] reported SBM supplementation (378 g/kg) effects on distal intestine microbial community of Atlantic salmon. Principal component analysis (PCA) revealed correlations that fish fed SBM diet was correlated with Aeromonas VIb and Sporosarcina aquimarina, while Microbacterium, Pseudomonas, Lactococcus lactis sp. cremoris, and Aeromonas VIa were correlated with the FM-based diet. Reveco et al. [103] investigated the microbiota in the mid and distal intestine of Atlantic salmon fed FM and solvent extracted SBM (200 g/kg) by DGGE analysis. Results showed increased Lactococcus lactis subsp. lactis in the mid-intestine, while a reduction in Weissella confusa in the distal intestine of Atlantic salmon fed 20% solvent extracted SBM-contained diet. Hartviksen et al. [102] revealed no dietary effect of soy protein concentrate (SPC) on total autochthonous bacteria isolated from PI and total allochthonous and total autochthonous bacteria isolated from DI of Atlantic salmon by qPCR analysis. However, significant (p = 0.05) effect was observed regarding community composition. An increase was noticed in autochthonous Enterobacteriaceae, Bacilli-like, Lactobacillaceae, and Streptococcaceae in PI, and Bacilli-like and Streptococcaceae in DI by SPC feeding. In contrast, a significant (p = 0.05) decrease was revealed in Vibrionaceae in PI.
5.2. In cyprinid fish
Most of the literature available on the effects of different soy products on the gut microbiota are on salmonid fish, and less is known for other species. The possible reasons behind this might be due to the less susceptibility of non-salmonid fish to SBMIE and histological damage [39]. In cyprinid fish, like in grass carp, the effects of dietary SBM inclusion (1.3% by dry weight) were compared with the inclusion of casein meal (CM; 1.0% by dry weight) on the autochthonous gut microbiota [105]. After 8 weeks of feeding, 16S rRNA PCR-DGGE analysis revealed a clear difference between the microbiota of the SBM group and the CM group with similarity between the groups of only 26% (p < 0.05). Unique bacteria isolated from the CM group were identified as follows: uncultured Lachnospiraceae bacterium, uncultured Lactobacillus, uncultured Clostridium spp., and uncultured Proteobacterium, while bacteria isolated from the SBM group were identified as Pseudomonas sp., Aeromonas sp., uncultured bacteria, uncultured Actinobacterium, and uncultured Bacillus spp.
Raggi and Gatlin [107] evaluated four probiotics diets based on FM and SBM on gut microbiota of goldfish (Carassius auratus). After 8 weeks of feeding, denaturing gradient gel electrophoresis (DGGE) analysis results revealed no difference in gut microbiota. The probable reason explained for this observation is due to the incorporation of dietary chromic oxide (10 g kg−1) which may have reduced the quantity and complexity of the bacterial community as reported by Ringø [112] for Arctic charr (Salvelinus alpinus L.). Cai et al. [106] also reported no significant effects of fishmeal replacement by SBM (30%) on the levels of total aerobic bacteria, total anaerobic bacteria, presumptive E. coli, Aeromonas, Bifidobacterium, or Clostridium in the intestine of silver crucian carp (Carassius auratus gibelio × Cyprinus carpio). Recently, the effect of partial replacement of SBM (4%) by intestinal casing meal (ICM), prepared from the wastewater of enteric coating and heparin processing, was used to evaluate the effect on the allochthonous gut microbiota of three cage-cultured cyprinid species [108]. Results indicated that the allochthonous bacterial diversity was altered by ICM substitution; however, by feeding ICM, some bacterial species were significantly stimulated, E. coli, and Exiguobacterium in black carp (Mylopharyngodon piceus) and species belonging to Firmicutes, Fusobacteria, and Proteobacteria in gibel carp (Carassius gebelio).
5.3. Cichlids and others
The effects of replacing dietary SBM or cottonseed meal (CSM) by completely hydrolyzed feather meal (CHFM) on the composition of gut microbiota was investigated by Zhang et al. [109] for hybrid tilapia. After 8 weeks of feeding, 16S rRNA PCR-DGGE analysis results revealed that CHFM induced modulation of the whole intestinal microbiota in hybrid tilapia and prevented colonization of potentially harmful species in the intestinal tract. Plesiomonas sp. BTOK4 and Aeromonas aquarium were found in decreased level in diet group where 120 g kg−1 CSM was replaced with CHFM. Miao et al. [80] reported the substitution effects of dietary SBM on the intestinal microbial community of northern snakehead. After 63-day feeding, trial results indicated that dietary soybean meal substitutions significantly affected the intestinal microbiota composition of fish. At the phylum level, Firmicutes abundance was the lowest in the diet group having 75% defatted fishmeal replacement with SBM, in contrast with Proteobacteria, Bacteroidetes, and Planctomycetes. At the genus level, significantly lower abundance of Lactococcus, Geobacillus, Pseudomonas, Streptococcus, Bacillus, and Acinetobacter, but higher abundance of Cetobacterium, Planctomyces, Shewanella, Thermomonas, Rubrivivax, and Carnobacterium was observed in fish fed the same diet group (75% defatted fishmeal replacement with SBM).
From previous research, it is established that gut microbiota influences several physiological and immunological aspects of aquatic animals like development, digestion, nutrition, immunological functions, and disease resistance [113, 114]. The gut microbiota together with digestive enzymes, mucins, peristalsis, and epithelial barrier with tight junctions belongs to the so-called non-immune component of mucosal immunity [115]. Moreover, several previous research findings indicated that intestinal microbiota is required for full immune maturation [116, 117], inflammatory diseases [117, 118], and to increase the host’s resistance toward pathogenic invasion and infection [119]. However, until recently, research relating on the effects of soy protein inclusion in fish feed and their interaction among gut microbiota and immune responses is scarce. So, further research on the interaction effect on gut microbiota and innate immune system due to soy protein utilization are required for further confirmation of the usability of SBM.
The highest maximum exploitation of marine resources used to produce FM has enforced fish nutritionist to use alternative protein sources as FM substitute in aquafeed. Worldwide availability and relatively cheaper price make SBM as one of the suitable alternative ingredients in aquafeed. However, high proportion of soy protein sources inclusion in aquafeed may impair fish immunity, maturation, and functionality of the intestinal mucosa, the first line of defense, and damage the gastrointestinal tract. However, using the appropriate proportions of alternative protein sources as well as SBM provides not only the option of limiting harm, but also there is also an interesting possibility to enhance GI immunity and disease resistance. From the available literature, it is showed that non-salmonids are less susceptible on the effects of SBM on the gut microbiota as well as the gut health than salmonids species. Until today, research on the effects of high soy protein inclusion in non-salmonid diets on gut health is little; so, more research warranted for non-salmonids fish. Future study is also needed on the use of different functional supplement in SBM-based diet to increase the efficiency of utilizing alternative protein (soy protein) through maintaining improved physiological and gut health condition. To date, most of the studies on SBM inclusion in aquafeed and its effects on fish intestinal microbiota were descriptive and only concerned the composition of the microbial community. Further works are warranted to investigate the functions of subpopulations in the microbiota and ultimately the functions to the species level due to alternative protein inclusion in aquafeed. In addition, the anaphylactic effects of SBM and the immune regulatory mechanisms involved merits further investigation.
We gratefully thank Dr. Nicholas Romano (University of Arkansas at Pine Bluff, Pine Bluff, AR, USA) for his help to make figure 3. The authors wish to acknowledge Ajinomoto Co. Inc. (Kanagawa, Japan) for their technical support to make histological slides for Amberjack.
1.Kumar V, Bledsoe J, Lee S, Romano N, Small BC, Lalgudi R, et al. Gut Microbiota Homoeostasis Maintains Via Changing the Distal Intestinal Morphology in Rainbow Trout Fed Soy Protein Based Diets. Unpublished; 2020a
2.Kumar V, Lee S, Cleveland B, Romano N, Lalgudi R, Rubio M, et al. Comparative evaluation of processed soybean meal (EnzoMealTM) vs. regular soybean meal as a fishmeal replacement in diets of rainbow trout (Oncorhynchus mykiss): Effects on growth performance and growth-related genes. Aquaculture. 2020b:516. DOI: 10.1016/j.aquaculture.2019.734652
3.Kumar V, Wang H-P, Lalgudi R, Cain R, McGraw B, Rosentrater KA. Processed soybean meal as an alternative protein source for yellow perch (Perca flavescens) feed. Aquaculture Nutrition. 2019;25(4):917-931
4.Refstie S, Korsøen ØJ, Storebakken T, Baeverfjord G, Lein I, Roem AJ. Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Aquaculture. 2000;190:49-63
5.Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony MN, Islam MJ, et al. Substitution of dietary fishmeal by soybean meal with inosine administration influences growth, digestibility, immunity, stress resistance and gut morphology of juvenile amberjack Seriola dumerili. Aquaculture. 2018;488:174-188
6.Baeverfjord G, Krogdahl Å. Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: A comparison with the intestines of fasted fish. J. Journal of Fish Diseases. 1996;19:375-387
7.Burrells C, Williams PD, Southgate PJ, Crampton VO. Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Veterinary Immunology and Immunopathology. 1999a;72:277-288
8.Chen W, Ai Q, Mai K, Xu W, Liufu Z, Zhang W, et al. Effects of dietary soybean saponins on feed intake, growth performance, digestibility and intestinal structure in juvenile Japanese flounder (Paralichthys olivaceus). Aquaculture. 2011;318:95-100
9.Deng J, Mai K, Ai Q, Zhang W, Wang X, Xu W, et al. Effects of replacing fish meal with soy protein concentrate on feed intake and growth of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture. 2006;258:503-513
10.Kaushik SJ, Cravedi JP, Lalles JP, Sumpter J, Fauconneau B, Laroche M. Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture. 1995;133:257-274
11.Krogdahl Å, Bakke-McKellep AM, Baeverfjord G. Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquaculture Nutrition. 2003;9:361-371
12.Li Y, Ai Q, Mai K, Xu W, Cheng Z. Effects of the partial substitution of dietary fish meal by two types of soybean meals on the growth performance of juvenile Japanese seabass, Lateolabrax japonicus (Cuvier 1828). Aquaculture Research. 2012;43:458-466
13.Barnes ME, Brown ML, Rosentrater KA, Sewell JR. An initial investigation replacing fish meal with a commercial fermented soybean meal product in the diets of juvenile rainbow trout. Open Journal of Animal Sciences. 2012;2:234-243
14.Chen L, Madl RL, Vadlani PV, Li L, Wang W. Chapter 8: Valueadded products from soybean: Removal of anti-nutritional factors via bioprocessing. In: El-Shemy HA, editor. Soybean Bio-Active Compounds. Rijeka, Croatia: InTechOpen; 2013
15.Zhou F, Song W, Shao Q, Peng X, Xiao J, Hua Y, et al. Partial replacement of fish meal by fermented soybean meal in diets for black sea bream, Acanthopagrus schlegelii, juveniles. Journal of the World Aquaculture Society. 2011;42:184-197
16.Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM. Important antinutrients in plant feedstuffs for aquaculture: An update on recent findings regarding responses in salmonids. Aquaculture Research. 2010;41:333-344
17.Barnes ME, Brown ML, Neiger R. Comparative performance of two rainbow trout strains fed fermented soybean meal. Aquaculture International. 2015;23:1227-1238
18.Kumar V, Makkar HPS, Becker K. Nutritional, physiological and haematological responses in rainbow trout (Oncorhynchus mykiss) juveniles fed detoxified Jatropha curcas kernel meal. Aquaculture Nutrition. 2011;17:451-467
19.Kumar V, Makkar HPS, Amselgruber W, Becker K. Physiological, haematological and histopathological responses in common carp (Cyprinus carpio L) fingerlings fed with differently detoxified Jatropha curcas kernel meal. Food and Chemical Toxicology. 2010;48:2063-2072
20.Merrifield DL, Olsen RE, Myklebust R, Ringo E. Dietary effect of soybean (Glycine max) products on gut histology and microbiota of fish. In: El-Shemy PH, editor. Soybean and Nutrition. Rijeka, Croatia: InTechOpen; 2011. pp. 231-250
21.Ringø E, Zhou Z, Gonzalez Vecino JL, Wadsworth S, Romero J, Krogdahl A, et al. Effects of dietary components on the gut microbiota of aquatic animals: A never-ending story? Aquaculture Nutrition. 2016a;22:219-282
22.Ringø E, Sperstad S, Myklebust R, Refstie S, Krogdahl A. Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.). Aquaculture. 2006;261:829-841
23.Ringø E, Zhou Z, Vecino JLG, Wadsworth S, Romero J, Krogdahl A, et al. Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquaculture Nutrition. 2016b;22:219-282
24.Cain K, Swan C. Barrier function and immunology. In: Martin Grosell APF, Colin JB, editors. Fish Physiology. Amsterdam, Netherlands: Academic Press; 2010. pp. 111-134
25.Gómez GD, Balcázar JL. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology. 2008;52(2):145-154. DOI: 10.1111/j.1574-695X.2007.00343.x
26.Liu Y et al. The protective role of glutamine on enteropathy induced by high dose of soybean meal in turbot, Scophthalmus maximus L. Aquaculture. 2018;497(5):510-519. DOI: 10.1016/j.aquaculture.2018.08.021
27.Kumar V. Jatropha meal and protein isolate as a protein source in aquafeed [PhD thesis]. Stuttgart, Germany: Department of Aquaculture Systems and Animal Nutrition, for Institute for Animal Productions in the Tropic and Subtropics, University of Hohenheim; 2011. Available from: https://opus.uni-hohenheim.de/volltexte/2011/628/pdf/PhD_thesis_Vikas_Kumar.pdf
28.Bai N et al. Protective effects of mannan oligosaccharides on turbot Scophthalmus maximus suffering from soy enteropathy. Aquaculture. 2017;476(February):141-151. DOI: 10.1016/j.aquaculture.2017.04.005
29.Bruce TJ, Neiger RD, Brown ML. Gut histology, immunology and the intestinal microbiota of rainbow trout, Oncorhynchus mykiss (Walbaum), fed process variants of soybean meal. Aquaculture Research. 2018;49:492-504
30.Gu M et al. Soybean meal induces enteritis in turbot Scophthalmus maximus at high supplementation levels. Aquaculture. 2016;464:286-295. DOI: 10.1016/j.aquaculture.2016.06.035
31.Jiang J, Shi D, Zhou X-Q, Hu Y, Feng L, Liu Y. In vitro and in vivo protective effect of arginine against lipopolysaccharide induced inflammatory response in the intestine of juvenile Jian carp (Cyprinus carpio var. Jian) fish. Shellfish Immunology. 2015a;42(2):457-464
32.Jiang WD et al. Dietary leucine regulates the intestinal immune status, immune-related signalling molecules and tight junction transcript abundance in grass carp (Ctenopharyngodon idella). Aquaculture. 2015b;444:134-142. DOI: 10.1016/j.aquaculture.2015.04.005
33.Zhao S et al. Citric acid mitigates soybean meal induced inflammatory response and tight junction disruption by altering TLR signal transduction in the intestine of turbot, Scophthalmus maximus L. Fish & Shellfish Immunology. 2019;92(March):181-187. DOI: 10.1016/j.fsi.2019.06.004
34.Buttle LG, Burrells AC, Good JE, Williams PD, Southgate PJ, Burrells C. The binding of soybean agglutinin (SBA) to the intestinal epithelium of Atlantic salmon Salmo salar and rainbow trout, Oncorhynchus mykiss, fed high levels of soybean meal. Veterinary Immunology and Immunopathology. 2001;80:237-244
35.Krogdahl A, Bakke-Mckellep AM, Roed KH, Baeverfjord G. Feeding Atlantic salmon Salmo salar L. soybean products: Effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquaculture Nutrition. 2000a;6:77-84
36.Van den Ingh T, Krogdahl Å, Olli JJ, Hendriks H, Koninkx J. Effects of soybean-containing diets on the proximal and distal intestine in Atlantic salmon (Salmo salar): A morphological study. Aquaculture. 1991;94:297-305
37.Van den Ingh TSGAM, Olli JJ, Krogdahl Å. Alcohol-soluble components in soybeans cause morphological changes in the distal intestine of Atlantic salmon, Salmo salar, L. Journal of Fish Diseases. 1996;19:47-53
38.Bakke-Mckellep AM, Press CM, Baeverfjord G, Krogdahl Å, Landsverk T. Changes in immune and enzyme histochemical phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal-induced enteritis. Journal of Fish Diseases. 2000;23:115-127
39.Zhou Z, Ringø E, Olsen RE, Song SK. Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: A review. Aquaculture Nutrition. 2018;24:644-665
40.Nordrum S, Bakke-McKellep AM, Krogdahl Å, Buddington RK. Effects of soybean meal and salinity on intestinal transport of nutrients in Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology. B. 2000;125:317-335
41.Urán PA. Etiology of soybean-induced enteritis in fish [PhD thesis]. The Netherlands: Wageningen University; 2008
42.Booman M, Forster I, Vederas JC, Groman DB, Jones SRM. Soybean meal-induced enteritis in Atlantic salmon (Salmo salar) and Chinook salmon (Oncorhynchus tshawytscha) but not in pink salmon (O. gorbuscha). Aquaculture. 2018;483:238-243
43.Cunningham KE, Turner JR. Myosin light chain kinase: Pulling the strings of epithelial tight junction function. Annals of the New York Academy of Sciences. 2013;1258(1):34-42. DOI: 10.1111/j.1749-6632.2012.06526.x.Myosin
44.Wang B et al. Glutamine and intestinal barrier function. Amino Acids. 2015;47(10):2143-2154. DOI: 10.1007/s00726-014-1773-4
45.Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Kader MA, et al. Effects of dietary administration of inosine on growth, immune response, oxidative stress and gut morphology of juvenile amberjack, Seriola dumerili. Aquaculture. 2017;468:534-544
46.Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Ono S, et al. Comparison of the effects of inosine and inosine monophosphate on growth, immune response, stress resistance and gut morphology of juvenile red sea bream, Pagrus major. Aquaculture. 2016;458:64-74
47.Refstie S, Landsverk T, Bakke-McKellep AM, Ringø E, Sundby A, Shearer KD, et al. Digestive capacity, intestinal morphology, and microflora of 1-year and 2-year old Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. Aquaculture. 2006;261:269-284
48.Sohrabnezhad M, Sudagar M, Mazandarani M. Effect of dietary soybean meal and multienzyme on intestine histology of beluga sturgeon (Huso huso). International Aquatic Research. 2017;9:271-280
49.Wang AR, Ran C, Ringø E, Zhou ZG. Progress in fish gastrointestinal microbiota research. Reviews in Aquaculture. 2018;10:626-640
50.Murashita K, Fukada H, Takahashi N, Hosomi N, Matsunari H, Furuita H, et al. Effect of feed ingredients on digestive enzyme secretion in fish. Bulletin of Japan Fisheries Research and Education Agency. 2015;40:69-74
51.Furutani T, Masumoto T, Fukada H. Response of cholecystokinin and digestive enzyme mRNA levels to various feed ingredients in yellowtail Seriola quinqueradiata. Fisheries Science. 2012;78:1075-1082
52.Perera E, Yúfera M. Effects of soybean meal on digestive enzymes activity, expression of inflammation-related genes, and chromatin modifications in marine fish (Sparus aurata L.) larvae. Fish Physiology and Biochemistry. 2017;43:563-578
53.Robaina L, Izquierdo MS, Moyano FJ, Socorro J, Vergara JM, Montero D, et al. Soybean and lupin seed meals as protein sources in diets for gilthead seabream (Sparus aurata): Nutritional and histological implications. Aquaculture. 1995;130:219-233
54.Santigosa E, Saenz de Rodriganez MA, Rodiles A, Barroso FG, Alarcon FJ. Effect of diets containing a purified soybean trypsin inhibitor on growth performance, digestive proteases and intestinal histology in juvenile sea bream (Sparus aurata L.). Aquaculture Research. 2010;41:187-198
55.Chikwati EM, Sahlmann C, Holm H, Penn MH, Krogdahl Å, Bakke AM. Alterations in digestive enzyme activities during the development of diet-induced enteritis in Atlantic salmon, Salmo salar L. Aquaculture. 2013;402-403:28-37
56.Lilleeng E, Froystad MK, Ostby GC, Valen EC, Krogdahl A. Effects of diets containing soybean meal on trypsin mRNA expression and activity in Atlantic salmon (Salmo salar L). Comparative Biochemistry and Physiology Part A. 2007;147:25-36
57.Byadgi O, Puteri D, Lee J-W, Chang T-C, Lee YH, Chu CY, et al. The effect of TLR9 agonist CpG oligodeoxynucleotides on the intestinal immune response of cobia (Rachycentron canadum). Journal of Immunology Research. 2014;2014:273284
58.Tafalla C, Leal E, Yamaguchi T, Fischer U. T cell immunity in the teleost digestive tract. Developmental and Comparative Immunology. 2016;64:167-177
59.Salinas I, Parra D. Fish mucosal immunity: Intestine. In: Beck B, Peatman E, editors. Mucosal Health in Aquaculture. 1st ed. Amsterdam, Netherlands: Elsevier; 2015. pp. 135-170
60.Fu GH, Bai ZY, Xia JH, Liu F, Liu P, Yue GH. Analysis of two lysozyme genes and antimicrobial functions of their recombinant proteins in Asian seabass. PLoS One. 2013;8:e79743
61.Sveinbjornsson B, Olsen R, Paulsen S. Immunocytochemical localization of lysozyme in intestinal eosinophilic granule cells of Atlantic salmon, Salmo salar L. Journal of Fish Diseases. 1996;19:349-355
62.Shen Y, Zhang J, Xu X, Fu J, Li J. Expression of complement component C7 and involvement in innate immune responses to bacteria in grass carp. Fish & Shellfish Immunology. 2012;33:448-454
63.Kania PW, Sorensen RR, Koch C, Brandt J, Kliem A, Vitved L, et al. Evolutionary conservation of mannan-binding lectin (MBL) in bony fish: Identification, characterization and expression analysis of three bona fide collectin homologues of MBL in the rainbow trout (Onchorhynchus mykiss). Fish & Shellfish Immunology. 2010;29:910-920
64.Lovoll M, Kilvik T, Boshra H, Bogwald J, Sunyer JO, Dalmo RA. Maternal transfer of complement components C3-1, C3-3, C3-4, C4, C5, C7, bf, and Df to offspring in rainbow trout (Oncorhynchus mykiss). Immunogenetics. 2006;58:168-179
65.Xia JH, Liu P, Liu F, Lin G, Sun F, Tu R, et al. Analysis of stress-responsive transcriptome in the intestine of Asian seabass (Lates calcarifer) using RNA-seq. DNA Research. 2013;20:449-460
66.Lokesh J, Fernandes JM, Korsnes K, Bergh O, Brinchmann MF, Kiron V. Transcriptional regulation of cytokines in the intestine of Atlantic cod fed yeast derived mannan oligosaccharide or beta-glucan and challenged with Vibrio anguillarum. Fish & Shellfish Immunology. 2012;33:626-631
67.Mulder IE, Wadsworth S, Secombes CJ. Cytokine expression in the intestine of rainbow trout (Oncorhynchus mykiss) during infection with Aeromonas salmonicida. Fish & Shellfish Immunology. 2007;23:747-759
68.Vasta GR, Nita-Lazar M, Giomarelli B, Ahmed H, Du S, Cammarata M, et al. Structural and functional diversity of the lectin repertoire in teleost fish: Relevance to innate and adaptive immunity. Developmental and Comparative Immunology. 2011;35:1388-1399
69.Casadei E, Bird S, Vecino JL, Wadsworth S, Secombes CJ. The effect of peptidoglycan enriched diets on antimicrobial peptide gene expression in rainbow trout (Oncorhynchus mykiss). Fish & Shellfish Immunology. 2013;34:529-537
70.Pan CY, Chen JY, Cheng YS, Chen CY, Ni IH, Sheen JF, et al. Gene expression and localization of the epinecidin-1 antimicrobial peptide in the grouper (Epinephelus coioides), and its role in protecting fish against pathogenic infection. DNA and Cell Biology. 2007;26:403-413
71.Seegert D, Rosenstiel P, Pfahler H, Pfefferkorna P, Nikolausa S, Schreibera S. Increased expression of IL-16 in inflammatory bowel disease. Gut. 2001;48:326-332
72.Vojtech LN, Scharping N, Woodson JC, Hansen JD. Roles of inflammatory caspases during processing of zebrafish interleukin-1b in Francisella noatunensis infection. Infection and Immunity. 2012;80(8):2878-2885
73.Larmonier CB, Uno JK, Lee KM, Karrasch T, Laubitz D, Thurston R, et al. Limited effects of dietary curcumin on Th-1 driven colitis in IL-10 deficient mice suggest an IL-10-dependent mechanism of protection. American Journal of Physiology. Gastrointestinal and Liver Physiology. 2008;295(5):G1079-G1091
74.Manzanillo P, Eidenschenk C, Ouyang W. Deciphering the crosstalk among IL-1 and IL-10 family cytokines in intestinal immunity. Trends in Immunology. 2015;36(8):471-478
75.Wang YR, Wang L, Zhang C-X, Song K. Effects of substituting fishmeal with soybean meal on growth performance and intestinal morphology in orange-spotted grouper (Epinephelus coioides). Aquaculture Report. 2017;5:52-57
76.Lilleeng E, Penn MH, Haugland O, Xu C, Bakke AM, Krogdahl A, et al. Decreased expression of TGF- beta, GILT and T- cell markers in the early stages of soybean enteropathy in Atlantic salmon (Salmo salar L.). Fish & Shellfish Immunology. 2009;27:65-72
77.Sahlmann C, Sutherland BJG, Kortner TM, Koop BF, Krogdahl Å, Bakke AM. Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. Fish & Shellfish Immunology. 2013;34:599-609
78.Kim DH, Austin B. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish & Shellfish Immunology. 2006;21:513-524
79.Marjara IS, Chikwati EM, Valen EC, Krogdahl Å, Bakke AM. Transcriptional regulation of IL-17A and other inflammatory markers during the development of soybean meal-induced enteropathy in the distal intestine of Atlantic salmon (Salmo salar L.). Cytokine. 2012;6:186-196
80.Miao S, Zhao C, Zhu J, Hu J, Dong X, Sun L. Dietary soybean meal affects intestinal homoeostasis by altering the microbiota, morphology and inflammatory cytokine gene expression in northern snakehead. Scientific Reports. 2018;8:113. DOI: 10.1038/s41598-017-18430-7
81.Gajardo K, Jaramillo-Torres A, Kortner TM, Merrifield DL, Tinsley J, Bakke AM, et al. Alternative protein sources in the diet modulate microbiota and functionality in the distal intestine of Atlantic Salmon (Salmo salar) Appl. Environmental Microbiology. 2017;83:e02615-e02616. DOI: 10.1128/AEM.02615-16
82.Austin B. The bacterial microflora of fish, revised. Scientific World Journal. 2006;6:931-945
83.Cahill MM. Bacterial flora of fishes: A review. Microbial Ecology. 1990;19:21-41
84.Hansen GH, Olafsen JA. Bacterial interactions in early life stages of marine cold water fish. Microbial Ecology. 1999;38:1-26
85.Horsley TW. A review of the bacterial flora of teleost and elasmobranchs, including methods for its analysis. Journal of Fish Biology. 1977;10:529-553
86.Izvekova GI, Izvekov EI, Plotnikov AO. Symbiotic microflora in fishes of different ecological groups. The Biological Bulletin. 2007;34:610-618
87.Llewellyn MS, Boutin S, Hoseinifar SH, Derome N. Teleost microbiomes: The state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Frontiers in Microbiology. 2014;5:207
88.Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RR, Bøgwald J, et al. The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture. 2010;302:1-18
89.Nya EJ, Austin B. Bacterial microflora of salmonids. In: Polakof S, Moon TW, editors. Trout: From Physiology to Conservation. New York: Nova Science Publishers, Inc.; 2013. pp. 113-129
90.Ringø E, Birkbeck TH. Intestinal microflora of fish larvae and fry. Aquaculture Research. 1999;30:73
91.Ringø E. Lactic acid bacteria in fish and fish farming. In: Salminen S, Ouwehand A, von Wright A, editors. Lactic Acid Bacteria. New York, NY, USA: Marcel Dekker Inc.; 2004. pp. 581-610
92.Yoshimizu M, Kimura T. Study on the intestinal microflora of salmonids. Fish Pathology. 1976;10:243-259
93.Kim D-H, Brunt J, Austin B. Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). Journal of Applied Microbiology. 2007;102:1654-1664
94.Heikkinen J, Vielma J, Kemilainen O, Tiirola M, Eskelinen P, Kiuru T, et al. Effects of soybean meal based diet on growth performance, gut histopathology and intestinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture. 2006;261:259-268
95.Merrifield DL, Bradley G, Baker RTM, Dimitroglou A, Davies SJ. Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) I. Effects on growth performance, feed utilisation, intestinal microbiota and related health criteria. Aquaculture Nutrition. Early View. 2009a;16:504-510 DOI: 10.1111/j.1365-2095.2009.00689.x
96.Mansfield GS, Desai AR, Nilson SA, Van Kessel AG, Drew MD, Hill JE. Characterization of rainbow trout (Oncorhynchus mykiss) intestinal microbiota and inflammatory marker gene expression in a recirculating aquaculture system. Aquaculture. 2010;307:95-104
97.Desai AR, Links MG, Collins SA, Mansfield GS, Drew MD, Van Kessel AG, et al. Effects of plant- based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture. 2012;350-353:134-142
98.Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, et al. Effects of dietary soybean meal, inulin and oxytetracycline on gastrointestinal histological characteristics, distal intestine cell proliferation and intestinal microbiota in Atlantic salmon (Salmo salar L.). British Journal of Nutrition. 2007;97:699-713
99.Ringø E, Sperstad S, Kraugerud OF, Krogdahl A. Use of 16S rRNA gene sequencing analysis to characterize culturable intestinal bacteria in Atlantic salmon (Salmo salar) fed diets with cellulose or non-starch polysaccharides from soy. Aquaculture Research. 2008a;39:1087-1100
100.Green TJ, Smullen R, Barnes AC. Dietary soybean protein concentrate- induced intestinal disorder in marine farmed Atlantic salmon, Salmo salar is associated with alterations in gut microbiota. Veterinary Microbiology. 2013;166:286-292
101.Navarrete P, Fuentes P, De la Fuentes L, Barros L, Magne F, Opazo R, et al. Short- term effects of dietary soybean meal and lactic acid bacteria on the intestinal morphology and microbiota of Atlantic salmon (Salmo salar). Aquaculture Nutrition. 2013;17:148-156
102.Hartviksen M, Gonzalez Vecino JL, Ringø E, Bakke A-M, Wadsworth S, Krogdahl Å, et al. Alternative dietary protein sources for Atlantic salmon (Salmo salar L.) affect intestinal microbiota, intestinal and liver histology and growth. Aquaculture Nutrition. 2014;20:381-398
103.Reveco FE, Øverland M, Romarheim OH, Mydland LT. Intestinal bacterial community structure differs between healthy and inflamed intestines in Atlantic salmon (Salmo salar L.). Aquaculture. 2014;420-421:262-269
104.Dimitroglou A, Merrifield DL, Spring P, Sweetman J, Moate R, Davies SJ. Effects of mannan oligosaccharides (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata). Aquaculture. 2010a;300:182-188
105.Huang G. The Study of Intestinal Bacterial Molecular Ecology of Cultured Fishes [master thesis]. Huazhong Agricultural University (in Chinese); 2008
106.Cai C-F, Wang W-J, Ye Y-T, Krogdahl Å, Wang Y-L, Xia Y-M, et al. Effect of soybean meal, raffinose and stachyose on the growth, body composition, intestinal morphology and intestinal microflora of juvenile allogynogenetic silver crucian carp (Carassius auratus ♀ x Cyprinus carpio ♂). Aquaculture Research. 2012;43:128-138
107.Raggi T, Gatlin DM III. Prebiotics have limited effects on nutrient digestibility of a diet based on fish meal and soybean meal in goldfish. North American Journal of Aquaculture. 2012;74:400-407
108.Li Z, Xu L, Liu W, Liu Y, Ringø E, Du Z, et al. Protein replacement in practical diets altered gut allochthonous bacteria of cultured cyprinid species with different food habits. Aquaculture International. 2015;23:913-928
109.Zhang Z, Xu L, Liu W, Yang Y, Du Z, Zhou Z. Effects of partial replacing soybean meal or cottonseed meal with completely hydrolysed feather meal (defatted rice bran as the carrier) on production, cytokines, adhesive gut bacteria, and disease resistance in hybrid tilapia (Oreochromis niloticus ♀ x Oreochromis aureus ♂). Fish & Shellfish Immunology. 2014;41:517-525
110.Tamboli CP, Neut C, Desreumaux P, Colombel JF. Dysbiosis as a prerequisite for IBD. Gut. 2004;53:1057
111.Turroni F, Ventura M, Buttó LF, Duranti S, O′Toole RW, Motherway MO, et al. Molecular dialogue between the human gut microbiota and the host: A Lactobacillus and Bifidobacterium perspective. Cellular and Molecular Life Sciences. 2014;71:183-203
112.Ringø E. Arctic charr, Salvelinus alpinus (L.), reared in fresh and sea water. An experimental study of lipid digestion and intestinal microflora [Ph.D. thesis]. Norway: Norwegian College of Fishery Science, University of Tromsø; 1993
113.Montalban-Arques A, De Schryver P, Bossier P, Gorkiewicz G, Mulero V, Gatlin DM III, et al. Selective manipulation of the gut microbiota improves immune status in vertebrates. Frontiers in Immunology. 2015;6:512. DOI: 10.3389/fimmu.2015.00512
114.Romero J, Ringø E, Merrifield DL. The gut microbiota of fish. In: Merrifield D, Ringø E, editors. Aquaculture Nutrition: Gut Health, Probiotics and Prebiotics. Oxford, UK: Wiley-Blackwell Publishing; 2014. pp. 75-100
115.Purchiaroni F, Tortora A, Gabrielli M, Bertucci F, Gigante G, Ianiro G, et al. The role of intestinal microbiota and the immune system. European Review for Medical and Pharmacological Sciences. 2013;17:323-333
116.Chung H, Pamp SJ, Hill J, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host- specific microbiota. Cell. 2012;149:1578-1593
117.Kamada N, Seo S-U, Chen GY, Núnez G. Role of the gut microbiota in immunity and inflammatory disease. Nature Reviews Immunology. 2013;13:321-335
118.Rendueles O, Ferrieres L, Fretaud M, Begaud E, Herbomel P, Levraud J-P, et al. A new zebrafish model of oro- intestinal pathogen colonization reveals a key role for adhesion in protection by probiotic bacteria. PLoS Pathogens. 2012;8:7. DOI: 10.1371/journal.ppat.1002815
119.De Schryver P, Vadstein O. Ecological theory as a foundation to control pathogenic invasion in aquaculture. ISME Journal. 2014;8:2360-2368
Written By
Vikas Kumar, Md. Sakhawat Hossain, Janice A. Ragaza and Marina Rubio Benito
Submitted: 12 August 2019Reviewed: 29 April 2020Published: 27 August 2020
Open access peer-reviewed chapter
