福尔摩斯白蚁肠道中纤维素分解原生生物与甲烷生成古细菌之间的共生关系。

IF 5.1 Q1 ECOLOGY ISME communications Pub Date : 2024-07-20 eCollection Date: 2024-01-01 DOI:10.1093/ismeco/ycae097
Masayuki Kaneko, Tatsuki Omori, Katsura Igai, Takako Mabuchi, Miho Sakai-Tazawa, Arisa Nishihara, Kumiko Kihara, Tsuyoshi Yoshimura, Moriya Ohkuma, Yuichi Hongoh
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摘要

厌氧原生生物经常携带产甲烷古菌,这些古菌显然通过消耗多余的 H2 来促进宿主的发酵代谢。然而,在许多情况下,内生甲烷菌的生态特性仍然难以捉摸。在这里,我们研究了白蚁后肠中的内共生甲烷菌(Cononympha protists)的生态学和基因组。显微镜和 16S rRNA 扩增子测序分析表明,一种名为 "Candidatus Methanobrevibacter cononymphae "的单一物种与 Cononympha leidyi 和 Cononympha koidzumii 都有关联,它在不同白蚁群落的 Cononympha 细胞中的感染率从 0.0% 到 99.8% 不等。精细的网络分析表明,多个 16S rRNA 序列变体共存于一个宿主细胞中,而且相同的变体同时存在于两种白蚁中,也存在于肠壁上。因此,"Ca.因此,"Ca. Methanobrevibacter cononymphae "是一种面生内共生菌,通过垂直传播与肠道环境频繁交换。事实上,透射电子显微镜显示了甲烷菌从或被锥穴细胞逃逸或吸收的情况。Ca.Ca.Methanobrevibacter cononymphae "的基因组显示出与其面生生活方式相一致的特征:即基因组大小(2.7 Mbp)与自由生活的亲缘菌相当;甲酸脱氢酶基因 fdhA 的假基因化,在不产生甲酸的宿主细胞中是不必要的;依赖宿主细胞中丰富的醋酸盐作为必要的碳源;存在过氧化氢酶基因,这是在微氧肠壁上定植所必需的。我们的研究揭示了甲烷菌与原生生物之间的多功能共生关系,这可能是一种应对白蚁肠道中不断变化的条件的策略。
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Facultative endosymbiosis between cellulolytic protists and methanogenic archaea in the gut of the Formosan termite Coptotermes formosanus.

Anaerobic protists frequently harbour methanogenic archaea, which apparently contribute to the hosts' fermentative metabolism by consuming excess H2. 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 Cononympha protists in the hindgut of the termite Coptotermes formosanus. Microscopic and 16S rRNA amplicon sequencing analyses revealed that a single species, designated here "Candidatus Methanobrevibacter cononymphae", is associated with both Cononympha leidyi and Cononympha koidzumii and that its infection rate in Cononympha 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 Cononympha species and also on the gut wall. Thus, "Ca. 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 Cononympha cell. The genome of "Ca. 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 fdhA, 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.

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