Ecological Specialization Within a Carnivorous Fish Family Is Supported by a Herbivorous Microbiome Shaped by a Combination of Gut Traits and Specific Diet

Escalas, Arthur; Auguet, Jean‐Christophe; Avouac, Amandine; Seguin, Raphaël; Gradel, Antoine; Borrossi, Lucie; Villéger, Sébastien

doi:10.3389/fmars.2021.622883

Cited by 51 publications

(41 citation statements)

References 64 publications

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“…Siganus rivulatus and S. luridus from Red Sea host gut microbiomes similar to the ones described for other Siganidae such as S. fuscescens from Australia [ 41 , 58 ], S. guttatus from Vietnamese coasts [ 44 ] and S. oramin from South-Eastern China [ 81 ]. The dominance of Firmicutes, Proteobacteria and Bacteroidetes phyla, and notably of the Ruminococcaceae, Desulfovibrionaceae, Rikenellaceae families, was associated with an herbivorous diet in several other fish families [ 27 , 55 , 75 ].…”

Section: Discussionmentioning

confidence: 99%

“…The bacterial phyla that decreased the most in abundance in the non-native range were the Firmicutes, with notably the Ruminococcaceae (UCG-014 genus), Erysipelotrichaceae ( Breznakia ) and Lachnospiraceae ( Bacteroides , Tyzerella ) families, and the Tennericutes. These taxa are well known members of herbivorous fish microbiome [ 27 , 55 , 68 , 75 ] because of their ability to anaerobically ferment plant polysaccharides to short chain fatty acids (SCFAs: acetate, formate, butyrate, propionate, valerate) thus transforming complex and indigestible polysaccharides into energy sources that can be absorbed by the host [ 25 , 66 , 72 , 80 ].…”

Section: Discussionmentioning

confidence: 99%

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Shift and homogenization of gut microbiome during invasion in marine fishes

et al. 2022

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Biological invasion is one of the main components of global changes in aquatic ecosystems. Unraveling how establishment in novel environments affects key biological features of animals is a key step towards understanding invasion. Gut microbiome of herbivorous animals is important for host health but has been scarcely assessed in invasive species. Here, we characterized the gut microbiome of two invasive marine herbivorous fishes (Siganus rivulatus and Siganus luridus) in their native (Red Sea) and invaded (Mediterranean Sea) ranges. The taxonomic and phylogenetic diversity of the microbiome increased as the fishes move away from the native range and its structure became increasingly different from the native microbiome. These shifts resulted in homogenization of the microbiome in the invaded range, within and between the two species. The shift in microbial diversity was associated with changes in its functions related with the metabolism of short-chain fatty acids. Altogether, our results suggest that the environmental conditions encountered by Siganidae during their expansion in Mediterranean ecosystems strongly modifies the composition of their gut microbiome along with its putative functions. Further studies should pursue to identify the precise determinants of these modifications (e.g. changes in host diet or behavior, genetic differentiation) and whether they participate in the ecological success of these species.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Shift and homogenization of gut microbiome during invasion in marine fishes

et al. 2022

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“…Recently, Escalas and coll. [ 113 ] highlighted that the dissimilarities between gut microbiota in sparids (study based on 12 species) were not explained by their phylogeny but by diet which appeared to be the most significant factor that directly affects the diversity and composition of fish gut microbiota [ 113 – 116 ]. Gut bacterial diversity is generally lower in carnivores, and increases in omnivores and herbivores [ 117 ], a trend also observed in the present study.…”

Section: Discussionmentioning

confidence: 99%

Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites

et al. 2022

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Background Animal-associated microbial communities appear to be key factors in host physiology, ecology, evolution and its interactions with the surrounding environment. Teleost fish have received relatively little attention in the study of surface-associated microbiota. Besides the important role of microbiota in homeostasis and infection prevention, a few recent studies have shown that fish mucus microbiota may interact with and attract some specific parasitic species. However, our understanding of external microbial assemblages, in particular regarding the factors that determine their composition and potential interactions with parasites, is still limited. This is the objective of the present study that focuses on a well-known fish-parasite interaction, involving the Sparidae (Teleostei), and their specific monogenean ectoparasites of the Lamellodiscus genus. We characterized the skin and gill mucus bacterial communities using a 16S rRNA amplicon sequencing, tested how fish ecological traits and host evolutionary history are related to external microbiota, and assessed if some microbial taxa are related to some Lamellodiscus species. Results Our results revealed significant differences between skin and gill microbiota in terms of diversity and structure, and that sparids establish and maintain tissue and species-specific bacterial communities despite continuous exposure to water. No phylosymbiosis pattern was detected for either gill or skin microbiota, suggesting that other host-related and environmental factors are a better regulator of host-microbiota interactions. Diversity and structure of external microbiota were explained by host traits: host species, diet and body part. Numerous correlations between the abundance of given bacterial genera and the abundance of given Lamellodiscus species have been found in gill mucus, including species-specific associations. We also found that the external microbiota of the only unparasitized sparid species in this study, Boops boops, harbored significantly more Fusobacteria and three genera, Shewenella, Cetobacterium and Vibrio, compared to the other sparid species, suggesting their potential involvement in preventing monogenean infection. Conclusions This study is the first to explore the diversity and structure of skin and gill microbiota from a wild fish family and present novel evidence on the links between gill microbiota and monogenean species in diversity and abundance, paving the way for further studies on understanding host-microbiota-parasite interactions.

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“…Despite the growing number of oral prophylactics being reported, the lack of consistency in performance, particularly on-site farm testing, and the limited successful application remain pressing issues ( 181 ). As the most diverse and largest vertebrate groups ( 182 ), fish display high heterogeneity in their physiology and immune system ( 38 ). For instance, the gadoid species do not possess CD4 ( 53 ) and MHC molecules ( 53 , 183 ) compared to the other finfish species.…”

Section: Challenges and Future Perspectivesmentioning

confidence: 99%

Gut Immune System and the Implications of Oral-Administered Immunoprophylaxis in Finfish Aquaculture

et al. 2021

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The gastrointestinal immune system plays an important role in immune homeostasis regulation. It regulates the symbiotic host-microbiome interactions by training and developing the host’s innate and adaptive immunity. This interaction plays a vital role in host defence mechanisms and at the same time, balancing the endogenous perturbations of the host immune homeostasis. The fish gastrointestinal immune system is armed with intricate diffused gut-associated lymphoid tissues (GALTs) that establish tolerance toward the enormous commensal gut microbiome while preserving immune responses against the intrusion of enteric pathogens. A comprehensive understanding of the intestinal immune system is a prerequisite for developing an oral vaccine and immunostimulants in aquaculture, particularly in cultured fish species. In this review, we outline the remarkable features of gut immunity and the essential components of gut-associated lymphoid tissue. The mechanistic principles underlying the antigen absorption and uptake through the intestinal epithelial, and the subsequent immune activation through a series of molecular events are reviewed. The emphasis is on the significance of gut immunity in oral administration of immunoprophylactics, and the different potential adjuvants that circumvent intestinal immune tolerance. Comprehension of the intestinal immune system is pivotal for developing effective fish vaccines that can be delivered orally, which is less labour-intensive and could improve fish health and facilitate disease management in the aquaculture industry.

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Ecological Specialization Within a Carnivorous Fish Family Is Supported by a Herbivorous Microbiome Shaped by a Combination of Gut Traits and Specific Diet

Cited by 51 publications

References 64 publications

Shift and homogenization of gut microbiome during invasion in marine fishes

Shift and homogenization of gut microbiome during invasion in marine fishes

Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites

Gut Immune System and the Implications of Oral-Administered Immunoprophylaxis in Finfish Aquaculture

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