Mei Ran, Kaneko Masanori, Imachi Hiroyuki, Nobu Masaru K
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba 305-8566, Japan.
Institute for Geo-Resources and Environment, Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba 305-8567, Japan.
PNAS Nexus. 2023 Jan 31;2(2):pgad023. doi: 10.1093/pnasnexus/pgad023. eCollection 2023 Feb.
Methanogenesis has been widely accepted as an ancient metabolism, but the precise evolutionary trajectory remains hotly debated. Disparate theories exist regarding its emergence time, ancestral form, and relationship with homologous metabolisms. Here, we report the phylogenies of anabolism-involved proteins responsible for cofactor biosynthesis, providing new evidence for the antiquity of methanogenesis. Revisiting the phylogenies of key catabolism-involved proteins further suggests that the last common ancestor (LACA) was capable of versatile H-, CO-, and methanol-utilizing methanogenesis. Based on phylogenetic analyses of the methyl/alkyl-S-CoM reductase family, we propose that, in contrast to current paradigms, substrate-specific functions emerged through parallel evolution traced back to a nonspecific ancestor, which likely originated from protein-free reactions as predicted from autocatalytic experiments using cofactor F. After LACA, inheritance/loss/innovation centered around methanogenic lithoautotrophy coincided with ancient lifestyle divergence, which is clearly reflected by genomically predicted physiologies of extant archaea. Thus, methanogenesis is not only a hallmark metabolism of , but the key to resolve the enigmatic lifestyle that ancestral archaea took and the transition that led to physiologies prominent today.
产甲烷作用已被广泛认为是一种古老的代谢方式，但精确的进化轨迹仍备受争议。关于其出现时间、原始形式以及与同源代谢的关系，存在不同的理论。在此，我们报告了负责辅因子生物合成的参与合成代谢的蛋白质的系统发育情况，为产甲烷作用的古老性提供了新证据。重新审视参与关键分解代谢的蛋白质的系统发育情况进一步表明，最后的共同祖先（LACA）能够进行多种利用氢气、一氧化碳和甲醇的产甲烷作用。基于甲基/烷基-S-辅酶M还原酶家族的系统发育分析，我们提出，与当前范式相反，底物特异性功能是通过可追溯到非特异性祖先的平行进化产生的，该祖先可能起源于使用辅因子F的自催化实验所预测的无蛋白质反应。在LACA之后，围绕产甲烷化无机自养的遗传/丢失/创新与古老的生活方式分化同时发生，这在现存古菌的基因组预测生理学中得到了明显体现。因此，产甲烷作用不仅是古菌的标志性代谢方式，也是解决祖先古菌所采取的神秘生活方式以及导致当今突出生理学特征的转变的关键。
