Baltic Sea methanogens compete with acetogens for electrons from metallic iron

Paola A. Palacios Jaramillo, Oona Snoeyenbos-West, Carolin Löscher, Bo Thamdrup, Amelia-Elena Rotaru*

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Resumé

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.

OriginalsprogEngelsk
TidsskriftI S M E Journal
Vol/bind13
Sider (fra-til)3011-3023
Antal sider13
ISSN1751-7362
DOI
StatusUdgivet - dec. 2019

Fingeraftryk

methanogens
Sporomusa
Baltic Sea
Iron
electrons
Electrons
iron
electron
Methanosarcina
acetate
Corrosion
corrosion
acetates
filtrates
Methane
methane production
Growth
methane
commensal
methanogenesis

Citer dette

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title = "Baltic Sea methanogens compete with acetogens for electrons from metallic iron",
abstract = "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.",
keywords = "microbial induced corrosion, Methanosarcina, Sporomusa, Bothnian Bay, Baltic Sea, iron corrosion, competition, interspecies interactions",
author = "{Palacios Jaramillo}, {Paola A.} and Oona Snoeyenbos-West and Carolin L{\"o}scher and Bo Thamdrup and Amelia-Elena Rotaru",
year = "2019",
month = "12",
doi = "10.1038/s41396-019-0490-0",
language = "English",
volume = "13",
pages = "3011--3023",
journal = "I S M E Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",

}

Baltic Sea methanogens compete with acetogens for electrons from metallic iron. / Palacios Jaramillo, Paola A.; Snoeyenbos-West, Oona; Löscher, Carolin; Thamdrup, Bo; Rotaru, Amelia-Elena.

I: I S M E Journal, Bind 13, 12.2019, s. 3011-3023.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Baltic Sea methanogens compete with acetogens for electrons from metallic iron

AU - Palacios Jaramillo, Paola A.

AU - Snoeyenbos-West, Oona

AU - Löscher, Carolin

AU - Thamdrup, Bo

AU - Rotaru, Amelia-Elena

PY - 2019/12

Y1 - 2019/12

N2 - 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.

AB - 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.

KW - microbial induced corrosion

KW - Methanosarcina

KW - Sporomusa

KW - Bothnian Bay

KW - Baltic Sea

KW - iron corrosion

KW - competition

KW - interspecies interactions

U2 - 10.1038/s41396-019-0490-0

DO - 10.1038/s41396-019-0490-0

M3 - Journal article

VL - 13

SP - 3011

EP - 3023

JO - I S M E Journal

JF - I S M E Journal

SN - 1751-7362

ER -