Although microbial humus respiration plays a critical role in organic matter decomposition and biogeochemical cycling of elements in diverse anoxic environments, the role of methane-producing species (methanogens) is not well defined. Here we report that a major fraction of humus, humic acid reduction enhanced the growth of Methanosarcina acetivorans above that attributed to methanogenesis when utilizing the energy sources methanol or acetate, results which showed both respiratory and fermentative modes of energy conservation. Growth characteristics with methanol were the same for an identically cultured mutant deleted for the gene encoding a multi-heme cytochrome c (MmcA), results indicating MmcA is not essential for respiratory electron transport to humic acid. Transcriptomic analyses revealed that growth with humic acid promoted the upregulation of genes annotated as cell surface pyrroloquinoline quinone (PQQ)-binding proteins. Furthermore, PQQ isolated from the membrane fraction was more abundant in humic acid-respiring cells, and the addition of PQQ improved efficiency of the extracellular electron transport. Given that the PQQ-binding proteins are widely distributed in methanogens, the findings extend current understanding of microbial humus respiration in the context of global methane dynamics.

尽管微生物腐殖质呼吸在不同缺氧环境中元素的有机物分解和生物地球化学循环中起着关键作用，但产生甲烷的物种（产甲烷菌）的作用尚未明确。在这里，我们报告了腐殖质的大部分，腐殖酸的还原在利用能源甲醇或乙酸盐时促进了甲烷生成的甲烷肉的生长，高于归因于甲烷生成的生长，结果显示了呼吸和发酵能量守恒模式。对于编码多血红素细胞色素 c （MmcA） 的基因缺失的相同培养突变体，甲醇的生长特性相同，结果表明 MmcA 对于呼吸电子向腐植酸的传输不是必需的。转录组学分析显示，腐植酸的生长促进了注释为细胞表面吡咯并喹啉醌 （PQQ） 结合蛋白的基因的上调。此外，从膜部分分离的 PQQ 在腐植酸呼吸细胞中更丰富，添加 PQQ 提高了细胞外电子传递的效率。鉴于 PQQ 结合蛋白广泛分布在产甲烷菌中，这些发现扩展了当前在全球甲烷动力学背景下对微生物腐殖质呼吸的理解。