期刊名称:Proceedings of the National Academy of Sciences
印刷版ISSN:0027-8424
电子版ISSN:1091-6490
出版年度:2022
卷号:119
期号:32
DOI:10.1073/pnas.2114799119
语种:English
出版社:The National Academy of Sciences of the United States of America
摘要:Significance
Wetlands are the major natural source of methane, an important greenhouse gas. The sulfur and methane cycles in wetlands are linked—e.g., a strong sulfur cycle can inhibit methanogenesis. Although there has historically been a clear distinction drawn between methane and sulfur oxidizers, here, we isolated a methanotroph that also performed respiratory oxidization of sulfur compounds. We experimentally demonstrated that thiotrophy and methanotrophy are metabolically compatible, and both metabolisms could be expressed simultaneously in a single microorganism. These findings suggest that mixotrophic methane/sulfur-oxidizing bacteria are a previously overlooked component of environmental methane and sulfur cycles. This creates a framework for a better understanding of these redox cycles in natural and engineered wetlands.
Natural and anthropogenic wetlands are major sources of the atmospheric greenhouse gas methane. Methane emissions from wetlands are mitigated by methanotrophic bacteria at the oxic–anoxic interface, a zone of intense redox cycling of carbon, sulfur, and nitrogen compounds. Here, we report on the isolation of an aerobic methanotrophic bacterium, ‘
Methylovirgula thiovorans' strain HY1, which possesses metabolic capabilities never before found in any methanotroph. Most notably, strain HY1 is the first bacterium shown to aerobically oxidize both methane and reduced sulfur compounds for growth. Genomic and proteomic analyses showed that soluble methane monooxygenase and XoxF-type alcohol dehydrogenases are responsible for methane and methanol oxidation, respectively. Various pathways for respiratory sulfur oxidation were present, including the Sox–rDsr pathway and the S
4I system. Strain HY1 employed the Calvin–Benson–Bassham cycle for CO
2 fixation during chemolithoautotrophic growth on reduced sulfur compounds. Proteomic and microrespirometry analyses showed that the metabolic pathways for methane and thiosulfate oxidation were induced in the presence of the respective substrates. Methane and thiosulfate could therefore be independently or simultaneously oxidized. The discovery of this versatile bacterium demonstrates that methanotrophy and thiotrophy are compatible in a single microorganism and underpins the intimate interactions of methane and sulfur cycles in oxic–anoxic interface environments.