{"title":"Cometabolism of ferrihydrite reduction and methyl-dismutating methanogenesis by <i>Methanosarcina mazei</i>.","authors":"Chaojie Guo, Yahai Lu","doi":"10.1128/aem.02238-24","DOIUrl":null,"url":null,"abstract":"<p><p>Recent discoveries have shown that some <i>Methanosarcina</i> species can reduce Fe(III), reshaping our understanding of <i>Methanosarcina</i> ecophysiology. However, the specific minerals reduced, the products formed, and the underlying metabolic mechanisms remain elusive. Here, we report on the cometabolic process of Fe(III) reduction and methylotrophic methanogenesis in <i>Methanosarcina mazei</i> zm-15. Biogeochemical and mineralogical analyses were conducted to investigate Fe(III) reduction from three mineral preparations-ferrihydrite, goethite, and hematite. The results revealed that 38% of the 6 mM Fe(III) in ferrihydrite was reduced within 4 days, and this percentage increased to 75% with the addition of 100 µM anthraquinone-2,6-disulfonate (AQDS). Active Fe(III) reduction occurred immediately and preceded rapid methanogenesis. The addition of ferrihydrite and AQDS together significantly enhanced the maximal CH₄ production rate. However, Fe(III) reduction did not occur in goethite or hematite, even with the addition of 100 µM AQDS. Vivianite was identified as the major product from ferrihydrite reduction. Transcriptomic analysis revealed that gene expression related to the oxidation branch of the methyl-dismutating pathway and the membrane-associated electron transport chain (ETC) was significantly upregulated, whereas the expressions of genes associated with the reduction branch of the methyl-dismutating pathway were downregulated. In conclusion, <i>M. mazei</i> zm-15 demonstrates a strong ability to reduce poorly crystalline ferrihydrite, but not highly crystalline goethite and hematite. During the cometabolism of Fe(III) reduction and CH₄ production from methanol, the methyl-oxidation and membrane ETC pathways are enhanced, while the methyl-reduction pathway is downregulated. The mechanism of electron relay from cells to ferrihydrite, however, remains unclear and warrants further investigation.IMPORTANCEThe recent discovery that certain <i>Methanosarcina</i> species can grow by reducing Fe(III) challenges the traditional understanding of methanogens. However, the underlying metabolic mechanisms remain largely unexplored. Using a combination of biogeochemical, mineralogical, and microbiological approaches, we investigated the ability of <i>Methanosarcina mazei</i> zm-15. It exhibited a strong capacity to reduce poorly crystalline ferrihydrite but not highly crystalline goethite and hematite. The formation of vivianite from ferrihydrite reduction is likely due to the high rate of Fe(III) reduction and the presence of excess phosphorus in incubations. During the cometabolism of Fe(III) reduction and CH<sub>4</sub> production from methanol, the methyl-oxidation and membrane electron transport pathways are upregulated, while the methyl-reduction pathway is downregulated. Our research uncovers a differential regulation of metabolic pathways during the cometabolism of Fe(III) reduction and CH<sub>4</sub> production from methanol. The findings shed new light on the adaptive strategies employed by <i>M. mazei</i> in environments with the presence of Fe(III) and suggestthat <i>Methanosarcina</i> can play a significant role in methane production and iron cycling in natural environments.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":" ","pages":"e0223824"},"PeriodicalIF":3.9000,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.02238-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Recent discoveries have shown that some Methanosarcina species can reduce Fe(III), reshaping our understanding of Methanosarcina ecophysiology. However, the specific minerals reduced, the products formed, and the underlying metabolic mechanisms remain elusive. Here, we report on the cometabolic process of Fe(III) reduction and methylotrophic methanogenesis in Methanosarcina mazei zm-15. Biogeochemical and mineralogical analyses were conducted to investigate Fe(III) reduction from three mineral preparations-ferrihydrite, goethite, and hematite. The results revealed that 38% of the 6 mM Fe(III) in ferrihydrite was reduced within 4 days, and this percentage increased to 75% with the addition of 100 µM anthraquinone-2,6-disulfonate (AQDS). Active Fe(III) reduction occurred immediately and preceded rapid methanogenesis. The addition of ferrihydrite and AQDS together significantly enhanced the maximal CH₄ production rate. However, Fe(III) reduction did not occur in goethite or hematite, even with the addition of 100 µM AQDS. Vivianite was identified as the major product from ferrihydrite reduction. Transcriptomic analysis revealed that gene expression related to the oxidation branch of the methyl-dismutating pathway and the membrane-associated electron transport chain (ETC) was significantly upregulated, whereas the expressions of genes associated with the reduction branch of the methyl-dismutating pathway were downregulated. In conclusion, M. mazei zm-15 demonstrates a strong ability to reduce poorly crystalline ferrihydrite, but not highly crystalline goethite and hematite. During the cometabolism of Fe(III) reduction and CH₄ production from methanol, the methyl-oxidation and membrane ETC pathways are enhanced, while the methyl-reduction pathway is downregulated. The mechanism of electron relay from cells to ferrihydrite, however, remains unclear and warrants further investigation.IMPORTANCEThe recent discovery that certain Methanosarcina species can grow by reducing Fe(III) challenges the traditional understanding of methanogens. However, the underlying metabolic mechanisms remain largely unexplored. Using a combination of biogeochemical, mineralogical, and microbiological approaches, we investigated the ability of Methanosarcina mazei zm-15. It exhibited a strong capacity to reduce poorly crystalline ferrihydrite but not highly crystalline goethite and hematite. The formation of vivianite from ferrihydrite reduction is likely due to the high rate of Fe(III) reduction and the presence of excess phosphorus in incubations. During the cometabolism of Fe(III) reduction and CH4 production from methanol, the methyl-oxidation and membrane electron transport pathways are upregulated, while the methyl-reduction pathway is downregulated. Our research uncovers a differential regulation of metabolic pathways during the cometabolism of Fe(III) reduction and CH4 production from methanol. The findings shed new light on the adaptive strategies employed by M. mazei in environments with the presence of Fe(III) and suggestthat Methanosarcina can play a significant role in methane production and iron cycling in natural environments.
期刊介绍:
Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.