Mechanisms for Electron Uptake by Methanosarcina acetivorans during Direct Interspecies Electron Transfer

Holmes, Dawn E.; Zhou, Junhu; Ueki, Toshiyuki; Woodard, Trevor L.; Lovley, Derek R.

doi:10.1128/mbio.02344-21

Cited by 53 publications

(60 citation statements)

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“…At least five different cyt c proteins are encoded in the M. acetivorans genome and these proteins contain between one and seven heme-binding motifs ( Holmes et al, 2019 ). Recent studies have even proposed distinct roles for some of these cyt c proteins in intracellular electron transport during methanogenesis ( Wang et al, 2011 ; Li et al, 2006 ; Schlegel et al, 2012 ; Ferry, 2020 ), extracellular electron transfer ( Holmes et al, 2019 ), as well as direct interspecies electron transfer between M. acetivorans and bacterial strains like Geobacter metallireducens ( Holmes et al, 2021 ). Thus, M. acetivorans is not only an ideal candidate to dissect the biogenesis of cyt c in Archaea but also to functionally characterize the role of cyt c in various electron transfer processes that have ramifications on global carbon cycling as well as on the formation of microbial communities in anoxic environments.…”

Section: Introductionmentioning

confidence: 99%

An Archaea-specific c-type cytochrome maturation machinery is crucial for methanogenesis in Methanosarcina acetivorans

Gupta

Shalvarjian

Nayak

2022

eLife

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C-type cytochromes (cyt c) are proteins that undergo post-translational modification to covalently bind heme, which allows them to facilitate redox reactions in electron transport chains across all domains of life. Genomic evidence suggests that cyt c are involved in electron transfer processes among the Archaea, especially in members that produce or consume the potent greenhouse gas methane. However, neither the maturation machinery for cyt c in Archaea nor their role in methane metabolism has ever been functionally characterized. Here, we have used CRISPR-Cas9 genome editing tools to map a distinct pathway for cyt c biogenesis in the model methanogenic archaeon Methanosarcina acetivorans, and have also identified substrate-specific functional roles for cyt c during methanogenesis. Although the cyt c maturation machinery from M. acetivorans is universally conserved in the Archaea, our evolutionary analyses indicate that different clades of Archaea acquired this machinery through multiple independent horizontal gene transfer events from different groups of Bacteria. Overall, we demonstrate the convergent evolution of a novel Archaea-specific cyt c maturation machinery and its physiological role during methanogenesis, a process which contributes substantially to global methane emissions

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Section: Introductionmentioning

confidence: 99%

An Archaea-specific c-type cytochrome maturation machinery is crucial for methanogenesis in Methanosarcina acetivorans

Gupta

Shalvarjian

Nayak

2022

eLife

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“…Recently, Holmes et al (2021) proposed a new model of DIET methanogenic pathways, which was confirmed in the defined co-culture of G. metallireducens and Methanosarcina acetivorans . Multiheme membrane-bound c-type cytochrome A (MmcA) in M. acetivorans played an important role in electron transfer.…”

Section: Challenges Of Direct Interspecies Electron Transfer In Anaer...mentioning

confidence: 84%

“…GAC did not make the co-culture system with MmcA-deficient strains produce methane rapidly, which was mainly because that MmcA was embedded in the cell membrane of M. acetivorans ( Ferry, 2020 ). Researches show that MmcA may exchange electrons with MP or rhodobacter nitrogen (Rnf) complex ( Suharti et al, 2014 ; Ferry, 2020 ; Holmes et al, 2021 ). The function of the Rnf is to accept electrons to produce the reduced ferredoxin, which is required for the first step in the reduction of CO 2 ( Holmes et al, 2021 ).…”

Section: Challenges Of Direct Interspecies Electron Transfer In Anaer...mentioning

confidence: 99%

“…Researches show that MmcA may exchange electrons with MP or rhodobacter nitrogen (Rnf) complex ( Suharti et al, 2014 ; Ferry, 2020 ; Holmes et al, 2021 ). The function of the Rnf is to accept electrons to produce the reduced ferredoxin, which is required for the first step in the reduction of CO 2 ( Holmes et al, 2021 ). The model in M. acetivorans is significantly different from that in M. barkeri , because M. Barkeri lack genes for MmcA and Rnf ( Zhou et al, 2021 ).…”

Section: Challenges Of Direct Interspecies Electron Transfer In Anaer...mentioning

confidence: 99%

“…The model in M. acetivorans is significantly different from that in M. barkeri , because M. Barkeri lack genes for MmcA and Rnf ( Zhou et al, 2021 ). Therefore, Methanogen growth via DIET may adopt different electron-acceptance strategies to accommodate these physiological differences ( Holmes et al, 2021 ).…”

Section: Challenges Of Direct Interspecies Electron Transfer In Anaer...mentioning

confidence: 99%

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Improvement of Direct Interspecies Electron Transfer via Adding Conductive Materials in Anaerobic Digestion: Mechanisms, Performances, and Challenges

Fang

Chang

et al. 2022

Front. Microbiol.

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Anaerobic digestion is an effective and sustainable technology for resource utilization of organic wastes. Recently, adding conductive materials in anaerobic digestion to promote direct interspecies electron transfer (DIET) has become a hot topic, which enhances the syntrophic conversion of various organics to methane. This review comprehensively summarizes the recent findings of DIET mechanisms with different mediating ways. Meanwhile, the influence of DIET on anaerobic digestion performance and the underlying mechanisms of how DIET mediated by conductive materials influences the lag phase, methane production, and system stability are systematically explored. Furthermore, current challenges such as the unclear biological mechanisms, influences of non-DIET mechanisms, limitations of organic matters syntrophically oxidized by way of DIET, and problems in practical application of DIET mediated by conductive materials are discussed in detail. Finally, the future research directions for practical application of DIET are outlined.

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Different outer membrane c‐type cytochromes are involved in direct interspecies electron transfer to Geobacter or Methanosarcina species

Holmes

Zhou

Smith

et al. 2022

mLife

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Direct interspecies electron transfer (DIET) may be most important in methanogenic environments, but mechanistic studies of DIET to date have primarily focused on cocultures in which fumarate was the terminal electron acceptor. To better understand DIET with methanogens, the transcriptome of Geobacter metallireducens during DIET‐based growth with G. sulfurreducens reducing fumarate was compared with G. metallireducens grown in coculture with diverse Methanosarcina. The transcriptome of G. metallireducens cocultured with G. sulfurreducens was significantly different from those with Methanosarcina. Furthermore, the transcriptome of G. metallireducens grown with Methanosarcina barkeri, which lacks outer‐surface c‐type cytochromes, differed from those of G. metallireducens cocultured with M. acetivorans or M. subterranea, which have an outer‐surface c‐type cytochrome that serves as an electrical connect for DIET. Differences in G. metallireducens expression patterns for genes involved in extracellular electron transfer were particularly notable. Cocultures with c‐type cytochrome deletion mutant strains, ∆Gmet_0930, ∆Gmet_0557 and ∆Gmet_2896, never became established with G. sulfurreducens but adapted to grow with all three Methanosarcina. Two porin–cytochrome complexes, PccF and PccG, were important for DIET; however, PccG was more important for growth with Methanosarcina. Unlike cocultures with G. sulfurreducens and M. acetivorans, electrically conductive pili were not needed for growth with M. barkeri. Shewanella oneidensis, another electroactive microbe with abundant outer‐surface c‐type cytochromes, did not grow via DIET. The results demonstrate that the presence of outer‐surface c‐type cytochromes does not necessarily confer the capacity for DIET and emphasize the impact of the electron‐accepting partner on the physiology of the electron‐donating DIET partner.

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Mechanisms for Electron Uptake by Methanosarcina acetivorans during Direct Interspecies Electron Transfer

Cited by 53 publications

References 65 publications

An Archaea-specific c-type cytochrome maturation machinery is crucial for methanogenesis in Methanosarcina acetivorans

An Archaea-specific c-type cytochrome maturation machinery is crucial for methanogenesis in Methanosarcina acetivorans

Improvement of Direct Interspecies Electron Transfer via Adding Conductive Materials in Anaerobic Digestion: Mechanisms, Performances, and Challenges

Different outer membrane c‐type cytochromes are involved in direct interspecies electron transfer to Geobacter or Methanosarcina species

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