Several Trichonympha protist species in the termite gut have independently acquired Desulfovibrio ectosymbionts in apparently different stages of symbiosis. Here, we obtained the near-complete genome sequence of Desulfovibrio phylotype ZnDsv-02, which attaches to the surface of Trichonympha collaris cells, and compared it with a previously obtained genome sequence of ‘Candidatus Desulfovibrio trichonymphae’ phylotype Rs-N31, which is almost completely embedded in the cytoplasm of Trichonympha agilis. 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.

白蚁肠道中的几种原生生物物种在明显不同的共生阶段独立获得了脱硫弧菌外共生体。在这里，我们获得了附着在Trichonymphae细胞表面的Desulfovibrio系统发育型ZnDsv-02的近乎完整的基因组序列，并将其与之前获得的“ Candidatus Desulfovibrio trichonymphae”系统发育型Rs-N31的基因组序列进行了比较，后者几乎与完全嵌入Trichonympha agilis的细胞质中。单核苷酸多态性分析表明，虽然Rs-N31几乎是克隆的，但单个宿主细胞上的ZnDsv-02群体是异质的。尽管存在这些差异，ZnDsv-02 的基因组已减少至 1.6 Mb，与 Rs-N31 (1.4 Mb) 相当，但与其他已知的原生生物外共生体不同，其基因组大小与其自由生活的近亲相似。除了 ZnDsv-02 中存在乳酸利用途径、细胞粘附成分和抗噬菌体防御系统外，两个基因组之间的整体基因丢失模式非常相似，包括对环境变化敏感的基因丢失。我们的研究表明，外共生体中可能会发生基因组减少，即使它们可以水平传播并通过横向转移获得基因，并且共生体基因组大小在很大程度上取决于它们在共生系统中的作用。