Functional diversity enables multiple symbiont strains to coexist in deep-sea mussels

Genetic diversity of closely related free-living microorganisms is widespread and underpins ecosystem functioning, but most evolutionary theories predict that it destabilizes intimate mutualisms. Accordingly, strain diversity is assumed to be highly restricted in intracellular bacteria associated with animals. Here, we sequenced metagenomes and metatranscriptomes of 18 Bathymodiolus mussel individuals from four species, covering their known distribution range at deep-sea hydrothermal vents in the Atlantic. We show that as many as 16 strains of intracellular, sulfur-oxidizing symbionts coexist in individual Bathymodiolus mussels. Co-occurring symbiont strains differed extensively in key functions, such as the use of energy and nutrient sources, electron acceptors and viral defence mechanisms. Most strain-specific genes were expressed, highlighting their potential to affect fitness. We show that fine-scale diversity is pervasive in Bathymodiolus sulfur-oxidizing symbionts, and hypothesize that it may be widespread in low-cost symbioses where the environment, rather than the host, feeds the symbionts.

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Supplementary Discussion, Supplementary Tables 1–5 and 7–11, and Supplementary Figs. 1–5.
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Reporting Summary
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Supplementary Table 6 List of strain-specific genes, excluding all hypothetical proteins.
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Source Data Fig. 2 Pi values per gene used in Permanova analysis and for Fig. 2a, as well as FST values used in Fig. 2b.
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Source Data Fig. 3 Source data for cumulative density plots and maximum strain numbers of 100× coverage (Fig. 3a) and source data for correlation of strain count with coverage (Fig. 3b).
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Source Data Fig. 4 Cumulative density data of strain counts for PacBio and Illumina Data for vent field Wideawake.
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Source Data Extended Data Fig. 5 Pi values per gene plotted in Extended Data Fig. 5.
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Source Data Extended Data Fig. 6 Source Data for correlation analysis of FST and SNP counts with mussel size, size sum and size differences.
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Source Data Extended Data Fig. 7 Source data for cumulative density plots and maximum strain numbers of full coverage, and phylaAmphora marker genes in full and 100× coverage.
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How to cite
Ansorge Rebecca, Romano Stefano, Sayavedra Lizbeth, Porras Miguel Angel Gonzalez, Kupczok Anne, Tegetmeyer Halina E., Dubilier Nicole, Petersen Jillian (2019). Functional diversity enables multiple symbiont strains to coexist in deep-sea mussels. Nature Microbiology. 4 (12). 2487-2497. https://doi.org/10.1038/s41564-019-0572-9, https://archimer.ifremer.fr/doc/00762/87404/

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