The life cycle of the deep-sea Bathymodiolus metaorganism: symbiont transmission and colonization of the host gill epithelium
Chemosynthetic symbioses evolved independently multiple times in at least nine animal phyla and from at least 12 lineages of free-living bacteria. They were first discovered at hydrothermal vents in the deep sea, and are also widespread in shallow marine habitats. Bathymodiolus mussels are one of the most abundant members of biological communities at marine hydrothermal vents and cold seeps. These hosts rely on a dense community of intracellular symbiotic bacteria in their gill epithelia that use reduced chemicals from the environment such as hydrogen sulfide and methane as an energy source to fix carbon dioxide or methane into biomass, which they pass on to feed their hosts. Bathymodiolus mussels are ideal for investigating the function and life history of symbiotic associations due to the relative simplicity of their symbiont community. Many Bathymodiolus species host two co-occurring symbionts, a single sulfur-oxidizing species and a single methane-oxidizing species. However, recent molecular studies and our preliminary metagenomic results have revealed that strain diversity within these two symbiont species is greater than previously assumed based on 16S rRNA gene analyses.
Here we propose to investigate this symbiont strain diversity and its effects on metaorganism function, development and evolution. Our investigation will include the study of strain distribution within the gill tissue of individual mussels (Sub-project 1) and the characterization of symbiont population structure across multiple individual mussels (Sub-project 2).
In our first sub-project, we will examine the strain diversity within individual mussels to better understand how these differ in their genomic and transcriptomic content, and thus function within the metaorganism using state-of-the art genomic technologies including single-cell genomics and a new method called Hi-C metagenomics. With these techniques we will be able to link distinct symbiont strains with mobile genetic elements such as phages and insertion sequences, which will provide insights into how these strains evolved. With in situ imaging, we plan to analyze the distribution patterns of distinct strains across an ontogenetic gradient within the host gill tissue, which will help to understand how the gill epithelium is colonized by symbionts throughout its lifetime.
In our second sub-project, we will investigate genomic diversity and evolution at the symbiont population level using high-resolution metagenomics. This in-depth metagenomic data will allow us to tease apart the effects of symbiont transmission mode, colonization history over the lifetime of the mussel, and symbiont diversification within a host individual, which together are the main factors driving symbiont community diversity in all host-microbe associations. With high-resolution metagenomes, we will investigate the selective forces acting on symbiont genomes by quantifying ratios of non-synonymous to synonymous substitutions.
This analysis will help to reveal the genomic mechanisms of symbiont adaptation to a host-associated lifestyle. Our research will lead to new insights into the ecology and evolutionary dynamics of symbiont acquisition and transmission mode, as well as a better understanding of the role of symbiont diversity in the ecology and evolution of metaorganisms.