A continuously changing selective context on microbial communities associated with fish, from egg to fork

Derôme, Nicolas; Filteau, Marie

doi:10.1111/eva.13027

Cited by 24 publications

(15 citation statements)

References 268 publications

(358 reference statements)

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“…Overall, results from other vertebrate model species (e.g. mouse, human, zebrafish, stickleback) showed that there are multiple ways in which the dialogue between two eukaryotic hosts can involve microbial communities: host–microbiota interactions, microbiota–microbiota interactions, and host–host interactions (reviewed in [ 39 , 40 ]).…”

Section: Discussionmentioning

confidence: 99%

Microbiomes of clownfish and their symbiotic host anemone converge before their first physical contact

et al. 2021

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Background One of the most charismatic, and yet not completely resolved example of mutualistic interaction is the partnership of clownfish and its symbiotic sea anemone. The mechanism explaining this tolerance currently relies on the molecular mimicry of clownfish epithelial mucus, which could serve as camouflage, preventing the anemone's nematocysts' discharge. Resident bacteria are known as key drivers of epithelial mucus chemical signature in vertebrates. A recent study has proposed a restructuration of the skin microbiota in a generalist clown fish when first contacting its symbiotic anemone. We explored a novel hypothesis by testing the effect of remote interaction on epithelial microbiota restructuration in both partners. Methods With metataxonomics, we investigated the epithelial microbiota dynamic of 18 pairs of percula clownfish (Amphiprion percula) and their symbiotic anemone Heteractis magnifica in remote interaction, physical interaction and control groups for both partners during a 4-week trial. Results The Physical and Remote Interaction groups’ results evidence gradual epithelial microbiota convergence between both partners when fish and anemone were placed in the same water system. This convergence occurred preceding any physical contact between partners, and was maintained during the 2-week interaction period in both contact groups. After the interaction period, community structure of both fish and anemone’s epthelial community structures maintained the interaction signature 2 weeks after fish–anemone pairs’ separation. Furthermore, the interaction signature persistence was observed both in the Physical and Remote Interaction groups, thus suggesting that water-mediated chemical communication between symbiotic partners was strong enough to shift the skin microbiota durably, even after the separation of fish–anemone pairs. Finally, our results suggest that fish–anemone convergent microbiota restructuration was increasingly associated with the parallel recruitment of three Flavobacteriaceae strains closely related to a tyrosinase-producing Cellulophaga tyrosinoxydans. Conclusions Our study shows that bacterial community restructuration, in the acclimation process, does not only rely on direct physical contact. Furthermore, our results challenge, for the first time, the traditional unidirectional chemical camouflage hypothesis, as we argue that convergence of the epithelial microbiota of both partners may play essential roles in establishing mutual acceptance.

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Section: Discussionmentioning

confidence: 99%

Microbiomes of clownfish and their symbiotic host anemone converge before their first physical contact

et al. 2021

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“…Gut microbial communities of fish shift with host development and living environments ( Yan et al, 2016 ; Lokesh et al, 2018 ; Derome and Filteau, 2020 ). Water is a living matrix in which many microbes reside, and it serves as a source for the fish gut microbiome ( Sun et al, 2019 ; Sehnal et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Quantifying the Colonization of Environmental Microbes in the Fish Gut: A Case Study of Wild Fish Populations in the Yangtze River

Yang

et al. 2022

Front. Microbiol.

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In aquatic animals, gut microbial communities shift with host development and living environments. Understanding the mechanism by which the environment impacts the gut microbial communities of aquatic animals is crucial for assessing and managing aquatic ecosystem health. Here, we proposed a simplified framework for the colonization and dynamics of gut microbial communities. Then, to quantify the colonization of environmental microbes in the wild fish gut, the current study used 16S rRNA gene amplicon sequencing to obtain the structure of the water environmental microbial community and the gut microbial community in 10 wild fish populations (Leiocassis crassilabris, Leiocassis longirostris, Pelteobagrus vachelli, Silurus asotus, Siniperca chuatsi, Coilia brachygnathus, Aristichthys nobilis, Hypophthalmichthys molitrix, Coreius heterodon, and Xenocypris argentea) from the Wuhan section of the Yangtze River, and the relationship of these microbial communities was analyzed. The results identified that in most individuals, approximately 80% of gut microbes [at the operational taxonomic unit (OTU) level] were shared with the water environmental microbial community (except for individuals of Siniperca chuatsi and Coilia brachygnathus, approximately 74%). In approximately 80% of individuals, more than 95% of microbial species (OTUs) in the gut were transient. For fish species, more than 99% of microbial species (OTUs) that were introduced into the gut were transient. Nearly 79% of OTUs and 89% of species of water environmental microbes could be introduced into the fish gut. Driven by the introduction of transient microbes, fishes with similar feeding habits had similar gut microbial communities. The results indicated that for adult wild fishes, most gut microbiota were transient from the environmental microbiota that were related to fish feeding habits. We therefore encourage future research to focus on environmental microbiota monitoring and management to promote the better conservation of aquatic animals. It was important to note that, because of various influence factors, interspecific differences and individual variations on gut microbial community characteristics, the quantification of gut microbes in the current work was approximate rather than accurate. We hope that more comparable research could be conducted to outline the quantitative characteristics of the relationship between gut microbial community and aquatic environment microbial community as soon as possible.

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“…However, the gut microbial community develops continuously during early life (yolk sac larvae–fry–fingerling) in a relatively harsh host–microbiome interaction environment under commercial aquaculture practices [ 8 ]. These pioneering microbes are particularly influential in the early life stage of the host, through fine tuning of host epigenetic patterns, and might therefore have a long term effect on the overall fitness of the host [ 9 – 11 ]. Therefore, the early environment may define the development and long-term fitness of the host via inoculation of the gut microbiome.…”

Section: Introductionmentioning

confidence: 99%

Impact of early-life rearing history on gut microbiome succession and performance of Nile tilapia

et al. 2021

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Background Fish gut microbial colonisation starts during larval stage and plays an important role in host’s growth and health. To what extent first colonisation could influence the gut microbiome succession and growth in later life remains unknown. In this study, Nile tilapia embryos were incubated in two different environments, a flow-through system (FTS) and a biofloc system (BFS); hatched larvae were subsequently cultured in the systems for 14 days of feeding (dof). Fish were then transferred to one common recirculating aquaculture system (RAS1, common garden, 15–62 dof), followed by a growth trial in another RAS (RAS2, growth trial, 63–105 dof). In RAS2, fish were fed with two types of diet, differing in non-starch polysaccharide content. Our aim was to test the effect of rearing environment on the gut microbiome development, nutrient digestibility and growth performance of Nile tilapia during post-larvae stages. Results Larvae cultured in the BFS showed better growth and different gut microbiome, compared to FTS. After the common garden, the gut microbiome still showed differences in species composition, while body weight was similar. Long-term effects of early life rearing history on fish gut microbiome composition, nutrient digestibility, nitrogen and energy balances were not observed. Still, BFS-reared fish had more gut microbial interactions than FTS-reared fish. A temporal effect was observed in gut microbiome succession during fish development, although a distinct number of core microbiome remained present throughout the experimental period. Conclusion Our results indicated that the legacy effect of first microbial colonisation of the fish gut gradually disappeared during host development, with no differences in gut microbiome composition and growth performance observed in later life after culture in a common environment. However, early life exposure of larvae to biofloc consistently increased the microbial interactions in the gut of juvenile Nile tilapia and might possibly benefit gut health.

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A continuously changing selective context on microbial communities associated with fish, from egg to fork

Cited by 24 publications

References 268 publications

Microbiomes of clownfish and their symbiotic host anemone converge before their first physical contact

Microbiomes of clownfish and their symbiotic host anemone converge before their first physical contact

Quantifying the Colonization of Environmental Microbes in the Fish Gut: A Case Study of Wild Fish Populations in the Yangtze River

Impact of early-life rearing history on gut microbiome succession and performance of Nile tilapia

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