A unique hydrogenase operon observed in the thioautotrophic symbiont of Bathymodiolus mussel in the East Pacific Rise

The mytilid mussel <em>Bathymodiolus thermophilus</em> lives in the deep-sea hydrothermal vent regions due to its symbiotic relationship with chemosynthetic Gammaproteobacteria species which reside inside specialized gill cells. It is well established that symbionts in the gill bacteriocytes utilize sulfur, methane and hydrogen available in the vent environment. However, some symbiont genomes of mussels either possess or lack genes for hydrogen metabolism within the single-ribotype population as well as host mussel species level. Here, we observed a unique hydrogenase operon consisting of additional H2-sensing hydrogenase subunits from a complete genome of <em>B. thermophilus</em> gill symbiont sampled from an individual mussel from the East Pacific Rise (EPR9N). Also, we found methylated regions sparsely distributed throughout the EPR9N genome, mainly in the transposases regions and densely present in the rRNA gene regions. CRISPR diversity analysis confirmed this genome originated from a single symbiont strain. Comparative analysis revealed that 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. Variation in genome size, gene content, and genome re-arrangements across individual hosts suggest 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 adaptive evolution of symbionts in deep-sea chemosynthetic environments.

深海热液贻贝（Bathymodiolus thermophilus）栖息于深海热液喷口区域，这得益于其与定殖于特化鳃细胞内的化能合成γ-变形菌纲（Gammaproteobacteria）细菌之间的共生关系。已有研究证实，鳃细菌细胞内的共生菌可利用喷口环境中的硫、甲烷与氢气。然而，在单核糖型种群乃至宿主贻贝物种层面，部分贻贝共生菌基因组的氢代谢相关基因存在有无差异。本研究从东太平洋海岭（EPR9N）的一只宿主贻贝中，获取了该深海热液贻贝鳃部共生菌的完整基因组，其中发现了一个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。同时，我们在EPR9N基因组中观察到分布不均的甲基化区域：主要稀疏分布于转座酶基因区域，而在核糖体RNA（rRNA）基因区域则呈现密集分布。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，该菌株与其他深海热液贻贝化能硫氧化鳃共生菌基因组共享2554个核心基因簇，另有125个基因簇为EPR9N菌株所特有。不同宿主个体间的基因组大小、基因组成及基因组重排情况存在差异，这表明深海热液贻贝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中共生菌的基因组结构演化、共生菌种群多样性及适应性演化相关的比较基因组学研究提供极为宝贵的研究资源。