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Isolation of Chitinolytic Bacteria from European Sea Bass Gut Microbiota Fed Diets with Distinct Insect Meals

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The ever-growing human population is increasingly demanding more fish. As a response, aquaculture has become the fastest growing industry in its sector. Alternatives to fish meal, an unsustainable commodity used as the main protein source for carnivorous species, are urgently needed in aquafeeds. Recently, in Europe, seven insect species have been approved as potential ingredients for animal feeds, including fish feed. However, chitin, one of the components of an insect’s exoskeleton, is indigestible for several economically valuable fish species, decreasing fish performance upon inclusion. This work aimed to isolate, from the European sea bass gastrointestinal tract, probiotic bacteria capable of producing chitinases to improve the use of diets containing high levels of insect meal. Based on the enhanced adaptability of gut microbial communities and the selective pressure of chitin-enriched diets on fish gut microbiota, bacteria were first isolated from the gastrointestinal tract of European sea bass fed chitin-enriched diets. Isolates were then comprehensively screened in vitro for important traits such as their ability to utilize chitin, gut-survival aptitude, and biosafety-related issues required to be considered eligible as probiotics by the European Food Safety Authority (EFSA).

Abstract

Insect meal (IM), recently authorized for use in aquafeeds, positions itself as a promising commodity for aquafeed inclusion. However, insects are also rich in chitin, a structural polysaccharide present in the exoskeleton, which is not digested by fish, resulting in lower fish performance. Through the application of a dietary pressure, this study aimed to modulate European sea bass gut microbiota towards the enrichment of chitinolytic bacteria to allow the isolation of novel probiotics capable of improving the use of IM-containing diets, overcoming chitin drawbacks. Five isoproteic (44%) and isolipidic (18%) diets were used: a fish meal (FM)-based diet (diet CTR), a chitin-supplemented diet (diet CHIT5), and three diets with either 25% of Hermetia illucens and Tenebrio molitor larvae meals (HM25 and TM25, respectively) or H. illucens exuviae meal (diet HEM25) as partial FM substitutes. After an 8-week feeding trial, the results showed a clear modulatory effect towards spore-forming bacteria by HM25 and HEM25 diets, with the latter being responsible for the majority of the chitinolytic fish isolates (FIs) obtained. Sequential evaluation of the FI hemolytic activity, antibiotic resistance, total chitinolytic activity, sporulation, and survival in gastrointestinal-like conditions identified FI645 and FI658 as the most promising chitinolytic probiotics for in vivo application.

SUBMITTER: Rangel F

PROVIDER: S-EPMC9312007 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The aquaculture industry is one of the fastest-growing sectors in animal food production. However, farming of carnivorous fish strongly relies on the use of wild fish-based meals, a practice that is environmentally and economically unsustainable. Insect-based diets constitute a strong candidate for fishmeal substitution, due to their high nutritional value and low environmental footprint. Nevertheless, data on the impact of insect meal (IM) on the gut microbiome of farmed fish are so far inconclusive, and very scarce in what concerns modulation of microbial-mediated functions. Here we use high-throughput 16S rRNA gene amplicon sequencing and quantitative PCR to evaluate the impact of different IMs on the composition and chitinolytic potential of the European sea bass gut digesta- and mucosa-associated communities. Our results show that insect-based diets of distinct origins differently impact the gut microbiota of the European sea bass (Dicentrarchus labrax). We detected clear modulatory effects of IM on the gut microbiota, which were more pronounced in the digesta, where communities differed considerably among the diets tested. Major community shifts were associated with the use of black soldier fly larvae (Hermetia illucens, HM) and pupal exuviae (HEM) feeds and were characterized by an increase in the relative abundance of the Firmicutes families Bacillaceae, Enterococcaceae, and Lachnospiraceae and the Actinobacteria family Actinomycetaceae, which all include taxa considered beneficial for fish health. Modulation of the digesta community by HEM was characterized by a sharp increase in Paenibacillus and a decrease of several Gammaproteobacteria and Bacteroidota members. In turn, a mealworm larvae-based diet (Tenebrio molitor, TM) had only a modest impact on microbiota composition. Further, using quantitative PCR, we demonstrate that shifts induced by HEM were accompanied by an increase in copy number of chitinase ChiA-encoding genes, predominantly originating from Paenibacillus species with effective chitinolytic activity. Our study reveals an HEM-driven increase in chitin-degrading taxa and associated chitinolytic activity, uncovering potential benefits of adopting exuviae-supplemented diets, a waste product of insect rearing, as a functional ingredient.

Project description:Vibrio anguillarum causes high mortality in European sea bass (Dicentrarchus labrax) larviculture and is a hindering factor for successful sustainable aquaculture of this commercially valuable species. Priming of the innate immune system through administration of immunostimulants has become an important approach to control disease outbreaks in marine fish larviculture. This study was conducted to evaluate immunostimulation by Escherichia coli HSP70 (DnaK) in axenic European sea bass larvae in order to protect the larvae against vibriosis. DnaK stimulates the immune response in crustaceans and juvenile fish against bacterial infections. The use of axenic fish larvae allows to study immunostimulation in the absence of an interfering microbial community. At 7 days post-hatching, larvae received a single dose of alginate encapsulated recombinant DnaK. Two non-treated control groups in which animals either received empty alginate microparticles (C1) or no alginante microparticles (C2 and C3) were included in the study. Eighteen hours later, all larvae, except the ones from group C3 (non-infected control) were challenged with V. anguillarum (105 CFU, bath infection). Mortality was daily recorded until 120 h post infection and at 18, 24, and 36 h post infection, larvae were sampled for expression of immune related genes. Results showed that V. anguillarum induced an immune response in axenic sea bass larvae but that the innate immune response was incapable to protect the larvae against deadly septicaemic disease. In addition, we showed that administration of alginate encapsulated DnaK to axenic European sea bass larvae at DAH7 resulted in a significant, DnaK dose dependent, upreglation of immune sensor, regulatory and effector genes. Significant upregulation of cxcr4, cas1 and especially of hep and dic was correlated with significant higher survival rates in V. anguillarum infected larvae. In the future recombinant DnaK might perhaps be used as a novel immunostimulant in sea bass larviculture.

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Isolation of Chitinolytic Bacteria from European Sea Bass Gut Microbiota Fed Diets with Distinct Insect Meals

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