Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature

Kokou, Fotini; Sasson, Goor; Nitzan, Tali; Doron‐Faigenboim, Adi; Harpaz, Sheenan; Cnaani, Avner; Mizrahi, Itzhak

doi:10.7554/elife.36398

Cited by 116 publications

(110 citation statements)

References 59 publications

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“…Hibernation and estivation processes may help the species to cope with unfavorable temperatures (Bullard et al, 2007;Ordóñez et al, 2015). Our results indicate that temperature adaptation seems to be a driving force in the colonization process of D. vexillum, and the microbiome can play a role in the thermal adaptation of the species, as has been suggested in fish and corals (Kokou et al, 2018;Osman et al, 2020).…”

Section: Discussionsupporting

confidence: 68%

The Microbiome of the Worldwide Invasive Ascidian Didemnum vexillum

Casso

Turon

Marco³

et al. 2020

Front. Mar. Sci.

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All multicellular organisms, including ascidians, host diverse microbial communities that are essential for their evolution. The global invader Didemnum vexillum is a colonial species native to Japan with two main genetic clades, A (the only invasive) and B, which provides a unique opportunity to assess if the microbiome remains stable in the colonization process or shifts according to local environment. We have analyzed, using 16S amplicon sequencing, the microbiome of 65 D. vexillum colonies from 13 populations worldwide including the two clades in the native area, plus samples from a congeneric species and seawater from one of the localities. We found 3,525 zeroradius operational taxonomic units (ZOTUs) in D. vexillum, belonging to 36 bacterial and 3 archaeal phyla. The microbiome of this species had a markedly different composition from surrounding seawater and from the congeneric species. For the globally invasive clade A, we found 3,154 ZOTUs, and 8 of them were present in all colonies, constituting a core microbiome with high abundance (69.57% of the total reads) but low diversity (0.25% of the total number of ZOTUs). The variable component was quantitatively much less important but comprised a highly diverse assemblage. In a multiple regression model, global microbiome structure correlated with differences in temperature range across localities and also with geographic distances, pointing to horizontal acquisition of the symbionts. However, the ascidian may have a strong capacity to select and enrich its microbiome, as we found that the most abundant ZOTUs from tunic samples had low abundance in seawater samples from the same locality. The microbiome structure also correlated with the genetic distances between colonies obtained in a previous genomewide analysis, suggesting some potential for vertical transmission. In geographically restricted comparisons, temperature and genetic makeup, but not geography, explained microbiome structure. The combination of a quantitatively dominant core component and a highly diverse variable fraction in the microbiome of D. vexillum can contribute to the success of this global invader in different environments.

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Section: Discussionsupporting

confidence: 68%

The Microbiome of the Worldwide Invasive Ascidian Didemnum vexillum

Casso

Turon

Marco³

et al. 2020

Front. Mar. Sci.

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“…Together these results indicate that the muscle-yield genetic lines are predictive of gut microbial assemblages and suggest that host genetic breeding might select for particular gut microbial assemblages. This notion is supported by recent studies in tilapia, showing host genetic selection effects for thermal tolerance on the microbiome composition [23]. Similarly, studies in stickleback fish identified association between gut microbial differences and host genetic divergence [24].…”

Section: Comparison Of Gut Assemblages In High-and Low-muscle Yield Gmentioning

confidence: 57%

Distinct Microbial Assemblages Associated with Genetic Selection for High- and Low- Muscle Yield in Rainbow Trout

Chapagain

Walker

Leeds

et al. 2020

Preprint

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Background Fish gut microbial assemblages play a crucial role in the growth rate, metabolism, and immunity of the host. We hypothesized that the gut microbiota of rainbow trout was correlated with breeding program based genetic selection for muscle yield. To test this hypothesis, fecal samples from 19 fish representing an F2 high-muscle genetic line (ARS-FY-H) and 20 fish representing an F1 low-muscle yield genetic line (ARS-FY-L) were chosen for microbiota profiling using the 16srRNA gene. Significant differences in microbial population between these two genetic lines might represent the effect of host genetic selection in structuring the gut microbiota of the host.Results Tukey’s transformed inverse Simpson indices indicated that ARS-FY-H samples have higher microbial diversity compared to those of the ARS-FY-L (LMM, χ2(1) = 14.11, p < 0.05). The fecal samples showed distinct clusters with significant differences in microbial assemblages between the genetic lines (F1,36= 4.7, p < 0.05, R2 = 11.9%). Further, Tax4Fun analyses predicted characteristic functional capabilities of the microbial communities in the ARS-FY-H and ARS-FY-L samples.Conclusion The significant differences of the microbial assemblages between ARS-FY-H and ARS-FY-L indicate an effect of genetic selection on the microbial diversity of the host. The functional composition of taxa demonstrates correlation of the function in improving the muscle accretion in the host, probably, by producing various metabolites and enzymes that might aid in digestion. Further research is required to elucidate the mechanisms involved in shaping the microbial community through host genetic selection.

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“…Variations in microbiota composition within the same species can be due to many factors. Differences in environment [46,52], season [48], age [36,50,51], sex [36], diet [18,42] or genetic background [53] can di cult comparisons among studies. In addition, technical differences, such as part of the intestine sampled [52,81], type of sample (adherent, transient or total microbiota) [82,83], DNA extraction techniques or analysis methodology [84,85], can also be a source of variation.…”

Section: Discussionmentioning

confidence: 99%

“…These studies were mainly focused on de ning baseline populations [35][36][37] or changes induced by diet [18,[38][39][40][41][42][43][44] or environmental conditions [45]. The microbiota is composed of very dynamic populations that are affected by different factors [18,36,[53][54][55]42,[46][47][48][49][50][51][52] such as diet, season, habitat, rearing density, age, sex and genetic background, the focus of the current study. There are not many studies de ning the effects of the host genome on intestinal microbiota composition in sh.…”

Section: Introductionmentioning

confidence: 99%

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

Piazzon

Naya-Català

Perera

et al. 2020

Preprint

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Background The key effects of intestinal microbiota in animal health has led to an increasing interest in manipulating these bacterial populations to improve animal welfare. The aquaculture sector is no exception and in the last years many studies have described these populations in different fish species. However, this is not an easy task, as intestinal microbiota is composed of very dynamic populations that are influenced by different factors, such as diet, environment, host age and genetics. In the current study, we aimed to determine whether the genetic background of gilthead sea bream ( Sparus aurata ) influences the intestinal microbial composition, how these bacterial populations are modulated by dietary changes, and the effect of selection by growth on intestinal disease resistance. To that aim, three different groups of five families of gilthead sea bream that were selected during two generations for fast, intermediate or slow growth (F3 generation) were kept together in the same open-flow tanks and fed a control or a well-balanced plant-based diet during nine months. Six animals per family and dietary treatment were sacrificed and the adherent bacteria from the anterior intestinal portion were sequenced. In parallel, fish of the fast- and slow-growth groups were infected with the intestinal parasite Enteromyxum leei and the disease signs, prevalence, intensity and parasite abundance were evaluated. Results No differences were detected in alpha diversity indexes among families, and the core bacterial architecture was the prototypical composition of gilthead sea bream intestinal microbiota, indicating no dysbiosis in any of the groups. The plant-based diet significantly changed the microbiota in the intermediate- and slow-growth families, with a much lower effect on the fast-growth group. Interestingly, the smaller changes detected in the fast-growth families potentially accounted for more changes at the metabolic level when compared to the other families. Upon parasitic infection, the fast-growth group showed significantly lower disease signs and parasite intensity and abundance than the slow-growth animals. Conclusions These results show a clear genome-metagenome interaction indicating that the fast-growth families harbor a microbiota that is more flexible upon dietary changes. These animals also showed a better ability to cope with intestinal infections.

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Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature

Cited by 116 publications

References 59 publications

The Microbiome of the Worldwide Invasive Ascidian Didemnum vexillum

The Microbiome of the Worldwide Invasive Ascidian Didemnum vexillum

Distinct Microbial Assemblages Associated with Genetic Selection for High- and Low- Muscle Yield in Rainbow Trout

Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream

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