Parallel reductive genome evolution in Desulfovibrio ectosymbionts independently acquired by Trichonympha protists in the termite gut

Several <i>Trichonympha</i> protist species in the termite gut have independently acquired <i>Desulfovibrio</i> ectosymbionts in apparently different stages of symbiosis. Here, we obtained the near-complete genome sequence of <i>Desulfovibrio </i>phylotype ZnDsv-02, which attaches to the surface of <i>Trichonympha collaris</i> cells, and compared it with a previously obtained genome sequence of ‘<i>Candidatus</i> Desulfovibrio trichonymphae’ phylotype Rs-N31, which is almost completely embedded in the cytoplasm of <i>Trichonympha agilis.</i> Single-nucleotide polymorphism analysis indicated that although Rs-N31 is almost clonal, the ZnDsv-02 population on a single host cell is heterogeneous. Despite these differences, the genome of ZnDsv-02 has been reduced to 1.6 Mb, which is comparable to that of Rs-N31 (1.4 Mb), but unlike other known ectosymbionts of protists with a genome similar in size to their free-living relatives. Except for the presence of a lactate utilization pathway, cell-adhesion components and anti-phage defense systems in ZnDsv-02, the overall gene-loss pattern between the two genomes is very similar, including the loss of genes responsive to environmental changes. Our study suggests that genome reduction can occur in ectosymbionts, even when they can be transmitted horizontally and obtain genes via lateral transfer, and that the symbiont genome size depends heavily on their role in the symbiotic system.<b></b>

白蚁肠道内的数种<italic>Trichonympha</italic>披发虫属（Trichonympha）原生动物，已独立获得隶属于<italic>Desulfovibrio</italic>脱硫弧菌属（Desulfovibrio）的外共生体（ectosymbionts），且二者的共生关系似乎处于不同的演化阶段。本研究获取了附着于<italic>Trichonympha collaris</italic>细胞表面的脱硫弧菌系统型（phylotype）ZnDsv-02的近完整基因组序列，并将其与此前获得的、几乎完全嵌入<italic>Trichonympha agilis</italic>细胞质内的‘<italic>Candidatus Desulfovibrio trichonymphae</italic> 候选脱硫弧菌披发虫（Candidatus Desulfovibrio trichonymphae）’系统型Rs-N31的基因组序列进行了比对分析。单核苷酸多态性（single-nucleotide polymorphism）分析结果显示，尽管Rs-N31种群几乎呈克隆性，但单个宿主细胞表面的ZnDsv-02种群具有异质性。尽管存在上述差异，ZnDsv-02的基因组已缩减至1.6 Mb，与Rs-N31的基因组大小（1.4 Mb）相当，但这与其他已知原生动物外共生体的基因组特征截然不同——后者的基因组尺寸与其自由生活的亲缘类群相近。除ZnDsv-02中存在乳酸利用通路、细胞黏附组分及抗噬菌体防御系统外，二者的整体基因丢失模式高度相似，包括对环境变化响应相关基因的丢失。本研究表明，即便外共生体可进行水平传播并通过侧向基因转移获取基因，其基因组仍可发生缩减；且共生体的基因组大小在很大程度上取决于其在共生系统中所承担的功能角色。