Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen

Prakash, Divya; Chauhan, Shikha S.; Ferry, James G.

doi:10.1126/sciadv.aaw9059

Cited by 57 publications

(81 citation statements)

References 44 publications

(57 reference statements)

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“…acetivorans (Yan et al, , b), and is believed to enable Ms . acetivorans performing the methanogenesis‐dependent respiration on ferrihydrite through extracellular electron transfer (Prakash et al ., ). Deletion of the membrane multiheme cytochrome A (MmcA) disrupts the respiratory growth of Ms .…”

Section: Resultsmentioning

confidence: 97%

“…Both types of methanogens have been routinely detected in environments such as rice paddy soils, natural wetlands, lake sediments and anaerobic digesters (Lyu and Liu, ). Recently, insightful understanding of aceticlastic methanogen ecophysiology has been revealed (Welte and Deppenmeier, ; Kulkarni et al ., ; Holmes et al ., ; Prakash et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…The Rhodobacter nitrogen fixation (Rnf) complex in Methanosarcina acetivorans is such a membrane‐associated oxidoreductase, which has been shown to catabolize in vitro reduction of soluble Fe 3+ and furthermore enable Ms . acetivorans performing respiratory growth on ferrihydrite (Yan et al, , b; Prakash et al ., ). The Ms .…”

Section: Introductionmentioning

confidence: 97%

“…The Ms . acetivorans in addition has the outer‐surface multiheme c ‐type cytochromes (MHC), which has been shown to play the essential role in extracellular electron transfer with humic‐like anthraquinone‐2,6‐disulfonate (AQDS) as the terminal electron acceptors or functioning as electron shuttles for the reduction of ferrihydrite (Holmes et al ., ; Prakash et al ., ). Therefore, it is likely that the aceticlastic methanogens like Ms .…”

Section: Introductionmentioning

confidence: 97%

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Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Wang

Byrne

Liu

et al. 2020

Environ Microbiol Rep

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It has been recently shown that magnetite nanoparticles (nanoFe 3 O 4 ) can facilitate methanogenic syntrophy but the effect of magnetite on methanogenesis alone remains elusive. Here we show that aceticlastic methanogenesis by Methanosarcina mazei is accelerated by magnetite and is correlated with the redox cycling of structural Fe(II) and Fe(III) in the mineral. An enrichment and its closest pure culture relative, Ms. mazei zm-15, both obtained from a natural wetland of the Tibetan plateau were tested in this experiment. The Fe(II) to Fe(III) ratios in magnetite, as measured by multiple approaches, show an initial increase in both the methanogenic cultures and the blank preparations containing no microbes. The Fe(II)/Fe(III) ratio then displays a distinct decline followed by an increase towards the end of incubation only in the enrichment and pure culture cultivations. This redox cycling of magnetite is in accordance with the stimulation of aceticlastic methanogenesis. Microscopic observation reveals the precipitation of nanoFe 3 O 4 on methanogen cell surface. The genomic analysis predicts that in addition to electron transfer components essential for aceticlastic methanogenesis, Ms. mazei zm-15 contains an outer-surface multiheme c-type cytochrome (MHC) and a few function-unknown surface proteins that harbour monoheme motif. We hypothesize that the redox cycling of nanoFe 3 O 4 delivers a positive influence via the MHC to the membrane electron transfer chain and hence promote the aceticlastic methanogenesis.

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Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

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Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Wang

Byrne

Liu

et al. 2020

Environ Microbiol Rep

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“…Furthermore, FldA replaced Fdx as an electron acceptor to the coenzyme F 420 H 2 -dependent electron bifurcating heterodisulfide reductase HdrA 2 B 2 C 2 (SI Appendix, Fig. S6) proposed to function in Fe(III)-dependent respiratory methanotrophic and acetotrophic growth of M. acetivorans (24,25). motif of FldA from M. acetivorans but are missing the cognate glycine residue that stabilizes the neutral sq in generic Flds (SI Appendix, Fig.…”

Section: Resultsmentioning

confidence: 99%

Structure and function of an unusual flavodoxin from the domain Archaea

Prakash

Iyer

Suharti

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Flavodoxins, electron transfer proteins essential for diverse metabolisms in microbes from the domainBacteria, are extensively characterized. Remarkably, although genomic annotations of flavodoxins are widespread in microbes from the domainArchaea, none have been isolated and characterized. Herein is described the structural, biochemical, and physiological characterization of an unusual flavodoxin (FldA) fromMethanosarcina acetivorans, an acetate-utilizing methane-producing microbe of the domainArchaea. In contrast to all flavodoxins, FldA is homodimeric, markedly less acidic, and stabilizes an anionic semiquinone. The crystal structure reveals an flavin mononucleotide (FMN) binding site unique from all other flavodoxins that provides a rationale for stabilization of the anionic semiquinone and a remarkably low reduction potentials for both the oxidized/semiquinone (−301 mV) and semiquinone/hydroquinone couples (−464 mV). FldA is up-regulated in acetate-grown versus methanol-grown cells and shown here to substitute for ferredoxin in mediating the transfer of low potential electrons from the carbonyl of acetate to the membrane-bound electron transport chain that generates ion gradients driving ATP synthesis. FldA offers potential advantages over ferredoxin by (i) sparing iron for abundant iron-sulfur proteins essential for acetotrophic growth and (ii) resilience to oxidative damage.

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Electrobiocorrosion by microbes without outer‐surface cytochromes

Holmes,

Woodard,

Smith

et al. 2024

mLife

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Anaerobic microbial corrosion of iron‐containing metals causes extensive economic damage. Some microbes are capable of direct metal‐to‐microbe electron transfer (electrobiocorrosion), but the prevalence of electrobiocorrosion among diverse methanogens and acetogens is poorly understood because of a lack of tools for their genetic manipulation. Previous studies have suggested that respiration with 316L stainless steel as the electron donor is indicative of electrobiocorrosion, because, unlike pure Fe0, 316L stainless steel does not abiotically generate H2 as an intermediary electron carrier. Here, we report that all of the methanogens (Methanosarcina vacuolata, Methanothrix soehngenii, and Methanobacterium strain IM1) and acetogens (Sporomusa ovata and Clostridium ljungdahlii) evaluated respired with pure Fe0 as the electron donor, but only M. vacuolata, Mx. soehngenii, and S. ovata were capable of stainless steel electrobiocorrosion. The electrobiocorrosive methanogens required acetate as an additional energy source in order to produce methane from stainless steel. Cocultures of S. ovata and Mx. soehngenii demonstrated how acetogens can provide acetate to methanogens during corrosion. Not only was Methanobacterium strain IM1 not capable of electrobiocorrosion, but it also did not accept electrons from Geobacter metallireducens, an effective electron‐donating partner for direct interspecies electron transfer to all methanogens that can directly accept electrons from Fe0. The finding that M. vacuolata, Mx. soehngenii, and S. ovata are capable of electrobiocorrosion, despite a lack of the outer‐surface c‐type cytochromes previously found to be important in other electrobiocorrosive microbes, demonstrates that there are multiple microbial strategies for making electrical contact with Fe0.

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Life on the thermodynamic edge: Respiratory growth of an acetotrophic methanogen

Cited by 57 publications

References 44 publications

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Redox cycling of Fe(II) and Fe(III) in magnetite accelerates aceticlastic methanogenesis by Methanosarcina mazei

Structure and function of an unusual flavodoxin from the domain Archaea

Electrobiocorrosion by microbes without outer‐surface cytochromes

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