Environmental conditions and neutral processes shape the skin microbiome of European catfish (<i>Silurus glanis</i>) populations of Southwestern France

Chiarello, Marlène; Paz‐Vinas, Ivan; Veyssière, Charlotte; Santoul, Frédéric; Loot, Géraldine; Ferriol, Jessica; Boulêtreau, Stéphanie

doi:10.1111/1758-2229.12774

Cited by 47 publications

(48 citation statements)

References 63 publications

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“…Amazon River fish were also found to have high Alphaproteobacteria under certain physicochemical conditions [31]. In stark contrast, Gammaproteobacteria dominated the skin microbiome in wild S. salar fry [24], and also that of Silurus glanis, catfish caught in the wild [16]. Of the five instances, the catfish is the only strictly-freshwater inhabitant, but it lacks scales.…”

Section: Freshwater Fish-skin Microbiomementioning

confidence: 99%

“…While most of the current research is targeted at fish species with commercial relevance [2,[26][27][28][29] or food safety [30], a few studies have dissected wild fish communities or populations, utilizing deep-sequencing culture-independent methods [15,16,31] and leaving the vast majority of wild habitats unexamined [32].…”

Section: Introductionmentioning

confidence: 99%

“…The skin microbiome is known to be affected by both environmental and fishspecies dependant factors [14,15], with evidence for co-phylogeny in coral reef fish [15]. On the population level, however, the existence of microbiome covariation with host genetics is inconsistent among systems [16][17][18].…”

Section: Introductionmentioning

confidence: 99%

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Dissecting the factors shaping fish skin microbiomes in a heterogeneous inland water system

Krotman

Yergaliyev

Alexander

et al. 2019

Preprint

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Fish skin microbiomes are rarely studied in inland water systems, in spite of their importance for fish health and ecology. This is mainly because fish species distribution often covaries with other biotic and abiotic factors, complicating the study-design. We tackled this issue in the northern part of the Jordan River system, in which a few fish species geographically overlap, across a steep gradients of water temperature and salinity. Using 16S rRNA metabarcoding, we studied the water properties that shape the skin bacterial communities, and their interaction with fish taxonomy. We found that considering the skin-community contamination by water microbial community is important, even when the water and skin communities are apparently different. With this in mind, we found alpha diversity of the skin-communities to be stable across sites, but higher in bentic loaches, compared to other fish.Beta diversity was found to be different among sites and to weakly covary with the dissolved oxygen, when treated skin-communities were considered. In contrast, water temperature and conductivity were strong factors explaining beta diversity in the untreated skin-communities. Beta diversity differences between co-occurring fish species emerged only for the treated skin-communities.Metagenomics predictions highlighted the microbiome functional implications of excluding the watercommunities contamination from the fish skin-communities. Finally, we found that human induced eutrophication promotes dysbiosis of the fish skin-community, with signatures relating to fish health. This finding was in line with recent studies, showing that biofilms capture sporadic pollution events, undetectable by interspersed water monitoring.

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Section: Freshwater Fish-skin Microbiomementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Dissecting the factors shaping fish skin microbiomes in a heterogeneous inland water system

Krotman

Yergaliyev

Alexander

et al. 2019

Preprint

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“…For instance, the stingrays were collected in the San Diego region, as were the leopard sharks; however, the stingray microbiomes were more similar to the whale shark microbiomes, which were collected in La Paz, Mexico (Supplemental table 1). Similar, environment has been shown to be linked with the skin microbiomes of teleost fishes [49,50] elasmobranchs [33], but these studies have focused on populations of a single species or biogeography, thus limiting insight into possible phylogenetic structure. Our study has leveraged several species, which exhibit varying geography, environment, and trophic positioning.…”

Section: Discussionmentioning

confidence: 99%

The skin microbiome of elasmobranchs follows phylosymbosis, but in teleost fishes the microbiomes converge

Doane

Morris

Papudeshi

et al. 2020

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Background: The vertebrate clade diverged into Chondrichthyes (sharks, rays, and chimeras) and Osteichthyes fishes (bony fishes) approximately 420 mya, with each group accumulating vast anatomical and physiological differences, including skin properties. The skin of Chondrichthyes fishes is covered in dermal denticles, whereas Osteichthyes fishes are covered in scales and are mucous rich. The divergence time among these two fish groups is hypothesized to result in predictable variation among symbionts. Here, using shotgun metagenomics, we test if patterns of diversity in the skin surface microbiome across the two fish clades match predictions made by phylosymbiosis theory. We hypothesize, 1) the skin microbiome will be species and clade-specific, 2) evolutionary difference in elasmobranch and teleost fishes corresponds with a concomitant increase in host-microbiome dissimilarity and 3) the skin structure of the two groups will affect the taxonomic and functional composition of the microbiomes. Results: We show that the taxonomic and functional composition of the microbiomes is host species-specific. Teleost fish had lower average microbiome within clade similarity compared to among clade comparison, but their composition is not different among clade in a null based model. Elasmobranch’s average similarity within clade was not different than across clade and not different in a null based model of comparison. In the comparison of host distance with microbiome distance, we found that the taxonomic composition of the microbiome was related to host distance for the elasmobranchs, but not the teleost fishes. In comparison, the gene function composition was not related to the host-organism distance for elasmobranchs but was negatively correlated with host distance for teleost fishes. Conclusion: Our results show the patterns of phylosymbiosis are not consistent across both fish clades, with the elasmobranchs showing phylosymbiosis, while the teleost fish are not. The discrepancy may be linked to alternative processes underpinning microbiome assemblage, including possible historical host-microbiome evolution of the elasmobranchs and convergent evolution in the teleost which filter specific microbial groups. Our comparison of the microbiomes among fishes represents an investigation into the microbial relationships of the oldest divergence extant vertebrate host and reveals that microbial relationships are not consistent across evolutionary timescales.

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“…The water microbiome of shponds were signi cantly distinct and more diverse than the skin and gill microbiomes of both sh, regardless of their age. It is known that free-living microbial communities retain higher richness than host-associated communities [31], with many studies showing a higher bacterial diversity in water relative to sh skin [28,30,36,[58][59][60], gills [14,36], gut [7,15,18,21,61], stomach [36], hindgut [36] and whole larvae [22]. Although some studies in sh have shown that the microbial communities found in the water tend to be recovered in the larval gut microbiome [17,21], others have also shown that water microbiomes do not in uence directly the microbiomes of sh mucosa [7, 8, 13-15, 18, 19, 22, 28, 30, 34, 36, 58-60, 62, 63].…”

Section: Fish and Water Microbiome Comparisonsmentioning

confidence: 99%

Characterization of the skin and gill microbiomes in farmed seabass and seabream across different age groups

Rosado

Pérez‐Losada

Pereira

et al. 2020

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Background Important changes in microbiome composition related to sexual maturation have been already reported in the gut of several vertebrates including mammals, amphibians and fish. Such changes in fish are linked to reproduction and growth during developmental stages, diet transitions and critical life events. We used amplicon (16S rRNA) high-throughput sequencing to characterize the skin and gill bacterial microbiomes of farmed seabass and seabream belonging to three different developmental age groups: early and late juveniles and mature adults. We also assessed the impact of the surrounding estuarine water microbiome in shaping the fish skin and gill microbiomes.Results Microbiome diversity, composition and potential metabolic functions varied across fish maturity stages. Alpha-diversity in the seabass microbiome varied significantly between age groups and was higher in older fish. Conversely, in the seabream, no significant differences were found in alpha diversity between age groups, although it was higher in the skin of juveniles. Microbiome structure varied significantly across age groups. Different bacterial metabolic pathways were predicted to be enriched in the microbiomes of both species. Finally, we found that the water microbiome is significantly distinct from all the fish microbiomes across the studied age groups, although a high percentage of ASVs is shared with the skin and gill microbiomes.Conclusions We report important microbial differences in composition and potential functionality across the different ages of farmed seabass and seabream. These differences may be related to somatic growth and the onset of sexual maturation. Importantly, some of the inferred metabolic pathways could enhance the host coping mechanisms during stressful conditions. Our results provide new evidence suggesting that growth and sexual maturation have an important role in shaping the external mucosa microbiomes of fish and highlight the importance of considering different life stages in microbiome studies.

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Environmental conditions and neutral processes shape the skin microbiome of European catfish (Silurus glanis) populations of Southwestern France

Cited by 47 publications

References 63 publications

Dissecting the factors shaping fish skin microbiomes in a heterogeneous inland water system

Dissecting the factors shaping fish skin microbiomes in a heterogeneous inland water system

The skin microbiome of elasmobranchs follows phylosymbosis, but in teleost fishes the microbiomes converge

Characterization of the skin and gill microbiomes in farmed seabass and seabream across different age groups

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