Kaneko Masayuki, Omori Tatsuki, Igai Katsura, Mabuchi Takako, Sakai-Tazawa Miho, Nishihara Arisa, Kihara Kumiko, Yoshimura Tsuyoshi, Ohkuma Moriya, Hongoh Yuichi
Department of Life Science and Technology, Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro-ku, Tokyo 152-8550, Japan.
Japan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074, Japan.
ISME Commun. 2024 Jul 20;4(1):ycae097. doi: 10.1093/ismeco/ycae097. eCollection 2024 Jan.
Anaerobic protists frequently harbour methanogenic archaea, which apparently contribute to the hosts' fermentative metabolism by consuming excess H. However, the ecological properties of endosymbiotic methanogens remain elusive in many cases. Here we investigated the ecology and genome of the endosymbiotic methanogen of the protists in the hindgut of the termite . Microscopic and 16S rRNA amplicon sequencing analyses revealed that a single species, designated here " Methanobrevibacter cononymphae", is associated with both and and that its infection rate in cells varied from 0.0% to 99.8% among termite colonies. Fine-scale network analysis indicated that multiple 16S rRNA sequence variants coexisted within a single host cell and that identical variants were present in both species and also on the gut wall. Thus, " Methanobrevibacter cononymphae" is a facultative endosymbiont, transmitted vertically with frequent exchanges with the gut environment. Indeed, transmission electron microscopy showed escape or uptake of methanogens from/by a cell. The genome of ". Methanobrevibacter cononymphae" showed features consistent with its facultative lifestyle: i.e., the genome size (2.7 Mbp) comparable to those of free-living relatives; the pseudogenization of the formate dehydrogenase gene , unnecessary within the non-formate-producing host cell; the dependence on abundant acetate in the host cell as an essential carbon source; and the presence of a catalase gene, required for colonization on the microoxic gut wall. Our study revealed a versatile endosymbiosis between the methanogen and protists, which may be a strategy responding to changing conditions in the termite gut.
厌氧原生生物常常携带着产甲烷古菌，这些古菌显然通过消耗过量的氢气来促进宿主的发酵代谢。然而，在许多情况下，内共生产甲烷菌的生态特性仍然难以捉摸。在此，我们研究了白蚁后肠中原生生物的内共生产甲烷菌的生态学和基因组。显微镜观察和16S rRNA扩增子测序分析表明，一种被命名为“共生短杆菌（Methanobrevibacter cononymphae）”的单一物种与两种原生生物都有关联，并且其在原生生物细胞中的感染率在不同白蚁群体中从0.0%到99.8%不等。精细尺度的网络分析表明，多个16S rRNA序列变体共存于单个宿主细胞内，并且相同的变体同时存在于两种原生生物物种以及肠壁上。因此，“共生短杆菌”是一种兼性内共生体，通过与肠道环境的频繁交换进行垂直传播。实际上，透射电子显微镜显示产甲烷菌从原生生物细胞中逸出或被原生生物细胞摄取。“共生短杆菌”的基因组显示出与其兼性生活方式相符的特征：即基因组大小（2.7 Mbp）与自由生活的亲缘物种相当；甲酸脱氢酶基因的假基因化，在不产生甲酸的宿主细胞内该基因是不必要的；依赖宿主细胞中丰富的乙酸盐作为必需碳源；以及存在过氧化氢酶基因，这是在微氧肠壁上定殖所必需的。我们的研究揭示了产甲烷菌与原生生物之间一种多样的内共生关系，这可能是对白蚁肠道中不断变化的条件做出的一种应对策略。
