Extracellular Electron Uptake by Two Methanosarcina Species

Yee, Mon Oo; Snoeyenbos-West, Oona; Thamdrup, Bo; Ottosen, Lars Ditlev Mørck; Rotaru, Amelia-Elena

doi:10.3389/fenrg.2019.00029

Cited by 84 publications

(55 citation statements)

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“…Nonetheless, Methanosarcina- species dominate on corroded Fe 0 -structures [7–10]. Therefore, we propose that Methanosarcina retrieves electrons directly from Fe 0 , extrapolating from recent findings that Methanosarcina can retrieve extracellular electrons directly from poised electrodes [29, 30], electrogenic syntrophic partners [31, 32], or electrically conductive particles [31–34]. Plausible scenarios for direct electron uptake in Methanosarcina have only recently been substantiated, using comparative transcriptomics [35].…”

Section: Introductionsupporting

confidence: 54%

“…Methanosarcina is the only known genus that includes species incapable of methanogenesis from H 2 [22, 25, 26], acetate [71], or both [23, 24]. Additionally, Methanosarcina includes species capable of direct electron uptake from electrodes [29, 30] and other cells either directly [29, 31, 32], or via conductive minerals [29, 31–34, 72]. The closest relative of Baltic- Methanosarcina was the non-acetoclastic and non-hydrogenotrophic M. subterranea (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Baltic Sea methanogens compete with acetogens for electrons from metallic iron

et al. 2019

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Microbially induced corrosion of metallic iron (Fe0)-containing structures is an environmental and economic hazard. Methanogens are abundant in low-sulfide environments and yet their specific role in Fe0 corrosion is poorly understood. In this study, Sporomusa and Methanosarcina dominated enrichments from Baltic Sea methanogenic sediments that were established with Fe0 as the sole electron donor and CO2 as the electron acceptor. The Baltic-Sporomusa was phylogenetically affiliated to the electroactive acetogen S. silvacetica. Baltic-Sporomusa adjusted rapidly to growth on H2. On Fe0, spent filtrate enhanced growth of this acetogen suggesting that it was using endogenous enzymes to retrieve electrons and produce acetate. Previous studies have proposed that acetate produced by acetogens can feed commensal acetoclastic methanogens such as Methanosarcina. However, Baltic-methanogens could not generate methane from acetate, plus the decrease or absence of acetogens stimulated their growth. The decrease in numbers of Sporomusa was concurrent with an upsurge in Methanosarcina and increased methane production, suggesting that methanogens compete with acetogens for electrons from Fe0. Furthermore, Baltic-methanogens were unable to use H2 (1.5 atm) for methanogenesis and were inhibited by spent filtrate additions, indicating that enzymatically produced H2 is not a favorable electron donor. We hypothesize that Baltic-methanogens retrieve electrons from Fe0 via a yet enigmatic direct electron uptake mechanism.

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Section: Introductionsupporting

confidence: 54%

Section: Resultsmentioning

confidence: 99%

Baltic Sea methanogens compete with acetogens for electrons from metallic iron

et al. 2019

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“…Methanogens differ in their H 2 threshold and H 2 affinity (Thauer et al, 2008) and a correlation between their H 2 threshold and Fe(0) corrosion rate was already suggested (Palacios Jaramillo, 2019). In addition, some methanogens were found to excrete hydrogenase enzymes to catalyze the H 2 evolution reaction (Deutzmann et al, 2015;Tsurumaru et al, 2018), while evidence exist that some methanogenic strains have a direct EET mechanism (Beese-Vasbender et al, 2015a;Rowe et al, 2019;Yee et al, 2019). Also the sulfate reducing IS4 strain likely has a direct EET mechanism (Beese-Vasbender et al, 2015b).…”

Section: Discussionmentioning

confidence: 99%

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Philips

2020

Front. Microbiol.

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Some acetogenic bacteria are capable of using solid electron donors, such as a cathode or metallic iron [Fe(0)]. Acetogens using a cathode as electron donor are of interest for novel applications such as microbial electrosynthesis, while microorganisms using Fe(0) as electron donor cause detrimental microbial induced corrosion. The capacity to use solid electron donors strongly differs between acetogenic strains, which likely relates to their extracellular electron transfer (EET) mechanism. Different EET mechanisms have been proposed for acetogenic bacteria, including a direct mechanism and a H 2 dependent indirect mechanism combined with extracellular hydrogenases catalyzing the H 2 evolution reaction on the cathode or Fe(0) surface. Interestingly, low H 2 partial pressures often prevail during acetogenesis with solid electron donors. Hence, an additional mechanism is here proposed: the maintenance of low H 2 partial pressures by microbial H 2 consumption, which thermodynamically favors the H 2 evolution reaction on the cathode or Fe(0) surface. This work elaborates how the H 2 partial pressure affects the H 2 evolution onset potential and the H 2 evolution rate on a cathode, as well as the free energy change of the anoxic corrosion reaction. In addition, the H 2 consumption characteristics, i.e., H 2 threshold (thermodynamic limit for H 2 consumption) and H 2 consumption kinetic parameters, of acetogenic bacteria are reviewed and evidence is discussed for strongly different H 2 consumption characteristics. Different acetogenic strains are thus expected to maintain different H 2 partial pressures on a cathode or Fe(0) surface, while those that maintain lower H 2 partial pressures (lower H 2 threshold, higher H 2 affinity) more strongly increase the H 2 evolution reaction. Consequently, I hypothesize that the different capacities of acetogenic bacteria to use solid electron donors are related to differences in their H 2 consumption characteristics. The focus of this work is on acetogenic bacteria, but similar considerations are likely also relevant for other hydrogenotrophic microorganisms.

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“…4). Regarding Methanosarcinales, their role in Fe 0 corrosion could be simply that of commensals feeding on the acetate generated by acetogens, or they could be involved in direct electron uptake from extracellular electron donors (Rotaru et al, 2014b, 2014a; Yee et al, 2019; Yee and Rotaru, 2020) including Fe 0 (Palacios et al, 2019a). However, direct electron uptake in Methanosarcinales is poorly understood and remains to be further investigated.…”

Section: Resultsmentioning

confidence: 99%

Opportunistic interactions on Fe⁰ between methanogens and acetogens from a climate lake

Rotaru

2019

Preprint

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10Urban environments are webbed with iron-steel structures above and belowground. Underground, in non-11 sulfidic environments, it has been suggested that interspecies interactions cause Fe 0 corrosion. Particularly, 12Methanosarcinales were assumed to interact syntrophically with acetogenic bacteria during Fe 0 corrosion. 13Here we challenge this assumption and show that a community of methanogens (38% Methanosarcinales) 14 prospers on Fe 0 especially after the demise of the acetogens. Acetogens were mainly represented by 15Clostridium (81% of Bacteria). Methanogens were however more diverse including Methanosarcina (22% of 16 Archaea), Methanosaeta (17% of Archaea) and Methanothermobacter (22% of Archaea) as key groups. 17 Surprisingly, acetogens started using electrons from Fe 0 immediately, unchallenged by competing 18 methanogens. Acetogens were expected to be outcompeted by energy efficient methanogens with 19 comparatively lower H2-uptake thresholds. However, acetogens prevailed, perhaps because in contrast to 20 methanogens they contain [FeFe]-hydrogenases (encoded in the lake-Clostridia metagenome).[FeFe]-21 hydrogenases from Clostridium were previously shown effective at retrieving electrons from Fe 0 for proton 22

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Extracellular Electron Uptake by Two Methanosarcina Species

Cited by 84 publications

References 56 publications

Baltic Sea methanogens compete with acetogens for electrons from metallic iron

Baltic Sea methanogens compete with acetogens for electrons from metallic iron

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Opportunistic interactions on Fe⁰ between methanogens and acetogens from a climate lake

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Extracellular Electron Uptake by Two Methanosarcina Species

Cited by 84 publications

References 56 publications

Baltic Sea methanogens compete with acetogens for electrons from metallic iron

Baltic Sea methanogens compete with acetogens for electrons from metallic iron

Extracellular Electron Uptake by Acetogenic Bacteria: Does H2 Consumption Favor the H2 Evolution Reaction on a Cathode or Metallic Iron?

Opportunistic interactions on Fe0 between methanogens and acetogens from a climate lake

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Opportunistic interactions on Fe⁰ between methanogens and acetogens from a climate lake