A complete genome of Bathymodiolus thermophilus thioautotrophic symbiont reveals a unique hydrogenase operon among hydrothermal vent mussel symbionts

The mytilid mussel <em>Bathymodiolus thermophilus</em> lives in the deep-sea hydrothermal vent regions thanks to its symbiotic relationship with chemosynthetic Gammaproteobacteria species which reside inside specialized gill cells. The symbionts in the gill bacteriocytes oxidize the reduced sulfur amply available in the vent environment. Here we sequenced and assembled the complete genome of a gill symbiont sampled from an individual mussel from the East Pacific Rise (EPR9N), using PacBio sequencing technology. The final symbiont assembly consists of a single contig size of 2.83 Mb, with a GC content of 38.6% and encodes for 2,133 protein-coding genes. CRISPR diversity analysis confirmed this genome is issued from a single symbiont strain. Comparative analysis revealed 2,554 core gene clusters were shared with other <em>B. thermophilus</em> thiotrophic gill symbiont genomes whereas 125 were unique to this EPR9N strain. In addition, we found that EPR9N strain has a unique hydrogenase operon among <em>Bathymodiolus</em> mussels consisting of additional H2-sensing hydrogenase subunits and a histidine kinase gene. Also, we found methylated regions distributed in patches throughout the EPR9N genome, mostly in the transposases regions and densely present in the rRNA gene regions. Variation in genome size, gene content and genome re-arrangements across individual hosts suggests multiple symbiont strains can associate with <em>B. thermophilus</em>. This complete mussel symbiont genome will be invaluable for further comparative genomic analyses studying structural genome evolution, symbiont population diversity, and symbiont ecology in the deep-sea chemosynthetic environments.

贻贝科（Mytilidae）的深海热液贻贝*Bathymodiolus thermophilus*，依托与栖息于其特化鳃细胞内的化能合成γ-变形菌纲（Gammaproteobacteria）物种的共生关系，得以在深海热液喷口区存活。鳃部菌胞内的共生菌可氧化喷口环境中大量存在的还原性硫化合物。本研究采用PacBio测序技术，对采自东太平洋海隆（East Pacific Rise, EPR9N）单一个体贻贝的鳃部共生菌完成了全基因组测序与组装。最终得到的共生菌基因组组装结果为一条长度2.83 Mb的重叠群（contig），GC含量为38.6%，共编码2133个蛋白质编码基因。CRISPR多样性分析证实该基因组仅来源于单一共生菌菌株。比较基因组分析显示，该菌株与其他*B. thermophilus*硫氧化型鳃共生菌的基因组共共享2554个核心基因簇，另有125个基因簇为EPR9N菌株所特有。此外，本研究发现EPR9N菌株在*Bathymodiolus*属贻贝中拥有独特的氢化酶操纵子，该操纵子包含额外的H₂感应氢化酶亚基以及一个组氨酸激酶基因。同时，研究人员在EPR9N基因组中发现呈斑块状分布的甲基化区域，这些区域主要位于转座酶编码区，并在rRNA基因区域呈现高密度分布。不同宿主个体间的基因组大小、基因组成以及基因组重排情况存在差异，这表明*B. thermophilus*可与多种共生菌菌株建立共生关系。这一完整的贻贝共生菌基因组，将为后续开展深海化能合成环境下的基因组结构演化、共生菌种群多样性以及共生菌生态学相关的比较基因组学研究提供极为宝贵的资源。