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Coming together-symbiont acquisition and early development in deep-sea bathymodioline mussels.

ABSTRACT: How and when symbionts are acquired by their animal hosts has a profound impact on the ecology and evolution of the symbiosis. Understanding symbiont acquisition is particularly challenging in deep-sea organisms because early life stages are so rarely found. Here, we collected early developmental stages of three deep-sea bathymodioline species from different habitats to identify when these acquire their symbionts and how their body plan adapts to a symbiotic lifestyle. These mussels gain their nutrition from chemosynthetic bacteria, allowing them to thrive at deep-sea vents and seeps worldwide. Correlative imaging analyses using synchrotron-radiation based microtomography together with light, fluorescence and electron microscopy revealed that the pediveliger larvae were aposymbiotic. Symbiont colonization began during metamorphosis from a planktonic to a benthic lifestyle, with the symbionts rapidly colonizing first the gills, the symbiotic organ of adults, followed by all other epithelia of their hosts. Once symbiont densities in plantigrades reached those of adults, the host's intestine changed from the looped anatomy typical for bivalves to a straightened form. Within the Mytilidae, this morphological change appears to be specific to Bathymodiolus and Gigantidas, and is probably linked to the decrease in the importance of filter feeding when these mussels switch to gaining their nutrition largely from their symbionts.

SUBMITTER: Franke M

PROVIDER: S-EPMC8370805 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Many foundation species in chemosynthesis-based ecosystems rely on environmentally acquired symbiotic bacteria for their survival. Hence, understanding the biogeographic distributions of these symbionts at regional scales is key to understanding patterns of connectivity and predicting resilience of their host populations (and thus whole communities). However, such assessments are challenging because they necessitate measuring bacterial genetic diversity at fine resolutions. For this purpose, the recently discovered clustered regularly interspaced short palindromic repeats (CRISPR) constitutes a promising new genetic marker. These DNA sequences harboured by about half of bacteria hold their viral immune memory, and as such, might allow discrimination of different lineages or strains of otherwise indistinguishable bacteria. In this study, we assessed the potential of CRISPR as a hypervariable phylogenetic marker in the context of a population genetic study of an uncultured bacterial species. We used high-throughput CRISPR-based typing along with multi-locus sequence analysis (MLSA) to characterize the regional population structure of the obligate but environmentally acquired symbiont species Candidatus Endoriftia persephone on the Juan de Fuca Ridge. Mixed symbiont populations of Ca. Endoriftia persephone were sampled across individual Ridgeia piscesae hosts from contrasting habitats in order to determine if environmental conditions rather than barriers to connectivity are more important drivers of symbiont diversity. We showed that CRISPR revealed a much higher symbiont genetic diversity than the other housekeeping genes. Several lines of evidence imply this diversity is indicative of environmental strains. Finally, we found with both CRISPR and gene markers that local symbiont populations are strongly differentiated across sites known to be isolated by deep-sea circulation patterns. This research showed the high power of CRISPR to resolve the genetic structure of uncultured bacterial populations and represents a step towards making keystone microbial species an integral part of conservation policies for upcoming mining operations on the seafloor.

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Coming together-symbiont acquisition and early development in deep-sea bathymodioline mussels.

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