Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates

Masahiko Morita, Nikhil S Malvankar, Ashley E Franks, Zarath M Summers, Ludovic Giloteaux, Amelia E Rotaru, Camelia Rotaru, Derek R Lovley, Amelia-Elena Rotaru

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

Mechanisms for electron transfer within microbial aggregates derived from an upflow anaerobic sludge blanket reactor converting brewery waste to methane were investigated in order to better understand the function of methanogenic consortia. The aggregates were electrically conductive, with conductivities 3-fold higher than the conductivities previously reported for dual-species aggregates of Geobacter species in which the two species appeared to exchange electrons via interspecies electron transfer. The temperature dependence response of the aggregate conductance was characteristic of the organic metallic-like conductance previously described for the conductive pili of Geobacter sulfurreducens and was inconsistent with electron conduction through minerals. Studies in which aggregates were incubated with high concentrations of potential electron donors demonstrated that the aggregates had no significant capacity for conversion of hydrogen to methane. The aggregates converted formate to methane but at rates too low to account for the rates at which that the aggregates syntrophically metabolized ethanol, an important component of the reactor influent. Geobacter species comprised 25% of 16S rRNA gene sequences recovered from the aggregates, suggesting that Geobacter species may have contributed to some but probably not all of the aggregate conductivity. Microorganisms most closely related to the acetate-utilizing Methanosaeta concilii accounted for more than 90% of the sequences that could be assigned to methane producers, consistent with the poor capacity for hydrogen and formate utilization. These results demonstrate for the first time that methanogenic wastewater aggregates can be electrically conductive and suggest that direct interspecies electron transfer could be an important mechanism for electron exchange in some methanogenic systems.
OriginalsprogEngelsk
TidsskriftmBio
Vol/bind2
Udgave nummer4
Sider (fra-til)e00159-11
ISSN2161-2129
DOI
StatusUdgivet - 2011

Fingeraftryk

Waste Water
Geobacter
Electrons
formic acid
Methane
Hydrogen
Sewage
rRNA Genes
Minerals
Ethanol

Citer dette

Morita, M., Malvankar, N. S., Franks, A. E., Summers, Z. M., Giloteaux, L., Rotaru, A. E., ... Rotaru, A-E. (2011). Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. mBio, 2(4), e00159-11. https://doi.org/10.1128/mBio.00159-11
Morita, Masahiko ; Malvankar, Nikhil S ; Franks, Ashley E ; Summers, Zarath M ; Giloteaux, Ludovic ; Rotaru, Amelia E ; Rotaru, Camelia ; Lovley, Derek R ; Rotaru, Amelia-Elena. / Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. I: mBio. 2011 ; Bind 2, Nr. 4. s. e00159-11.
@article{fa6dcbe78f5347bf9f5df0adf40ac60b,
title = "Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates",
abstract = "Mechanisms for electron transfer within microbial aggregates derived from an upflow anaerobic sludge blanket reactor converting brewery waste to methane were investigated in order to better understand the function of methanogenic consortia. The aggregates were electrically conductive, with conductivities 3-fold higher than the conductivities previously reported for dual-species aggregates of Geobacter species in which the two species appeared to exchange electrons via interspecies electron transfer. The temperature dependence response of the aggregate conductance was characteristic of the organic metallic-like conductance previously described for the conductive pili of Geobacter sulfurreducens and was inconsistent with electron conduction through minerals. Studies in which aggregates were incubated with high concentrations of potential electron donors demonstrated that the aggregates had no significant capacity for conversion of hydrogen to methane. The aggregates converted formate to methane but at rates too low to account for the rates at which that the aggregates syntrophically metabolized ethanol, an important component of the reactor influent. Geobacter species comprised 25{\%} of 16S rRNA gene sequences recovered from the aggregates, suggesting that Geobacter species may have contributed to some but probably not all of the aggregate conductivity. Microorganisms most closely related to the acetate-utilizing Methanosaeta concilii accounted for more than 90{\%} of the sequences that could be assigned to methane producers, consistent with the poor capacity for hydrogen and formate utilization. These results demonstrate for the first time that methanogenic wastewater aggregates can be electrically conductive and suggest that direct interspecies electron transfer could be an important mechanism for electron exchange in some methanogenic systems.",
keywords = "Archaea, Bacteria, Electron Transport, Methane, Molecular Sequence Data, Sewage",
author = "Masahiko Morita and Malvankar, {Nikhil S} and Franks, {Ashley E} and Summers, {Zarath M} and Ludovic Giloteaux and Rotaru, {Amelia E} and Camelia Rotaru and Lovley, {Derek R} and Amelia-Elena Rotaru",
year = "2011",
doi = "10.1128/mBio.00159-11",
language = "English",
volume = "2",
pages = "e00159--11",
journal = "mBio",
issn = "2161-2129",
publisher = "American Society for Microbiology",
number = "4",

}

Morita, M, Malvankar, NS, Franks, AE, Summers, ZM, Giloteaux, L, Rotaru, AE, Rotaru, C, Lovley, DR & Rotaru, A-E 2011, 'Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates', mBio, bind 2, nr. 4, s. e00159-11. https://doi.org/10.1128/mBio.00159-11

Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. / Morita, Masahiko; Malvankar, Nikhil S; Franks, Ashley E; Summers, Zarath M; Giloteaux, Ludovic; Rotaru, Amelia E; Rotaru, Camelia; Lovley, Derek R; Rotaru, Amelia-Elena.

I: mBio, Bind 2, Nr. 4, 2011, s. e00159-11.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates

AU - Morita, Masahiko

AU - Malvankar, Nikhil S

AU - Franks, Ashley E

AU - Summers, Zarath M

AU - Giloteaux, Ludovic

AU - Rotaru, Amelia E

AU - Rotaru, Camelia

AU - Lovley, Derek R

AU - Rotaru, Amelia-Elena

PY - 2011

Y1 - 2011

N2 - Mechanisms for electron transfer within microbial aggregates derived from an upflow anaerobic sludge blanket reactor converting brewery waste to methane were investigated in order to better understand the function of methanogenic consortia. The aggregates were electrically conductive, with conductivities 3-fold higher than the conductivities previously reported for dual-species aggregates of Geobacter species in which the two species appeared to exchange electrons via interspecies electron transfer. The temperature dependence response of the aggregate conductance was characteristic of the organic metallic-like conductance previously described for the conductive pili of Geobacter sulfurreducens and was inconsistent with electron conduction through minerals. Studies in which aggregates were incubated with high concentrations of potential electron donors demonstrated that the aggregates had no significant capacity for conversion of hydrogen to methane. The aggregates converted formate to methane but at rates too low to account for the rates at which that the aggregates syntrophically metabolized ethanol, an important component of the reactor influent. Geobacter species comprised 25% of 16S rRNA gene sequences recovered from the aggregates, suggesting that Geobacter species may have contributed to some but probably not all of the aggregate conductivity. Microorganisms most closely related to the acetate-utilizing Methanosaeta concilii accounted for more than 90% of the sequences that could be assigned to methane producers, consistent with the poor capacity for hydrogen and formate utilization. These results demonstrate for the first time that methanogenic wastewater aggregates can be electrically conductive and suggest that direct interspecies electron transfer could be an important mechanism for electron exchange in some methanogenic systems.

AB - Mechanisms for electron transfer within microbial aggregates derived from an upflow anaerobic sludge blanket reactor converting brewery waste to methane were investigated in order to better understand the function of methanogenic consortia. The aggregates were electrically conductive, with conductivities 3-fold higher than the conductivities previously reported for dual-species aggregates of Geobacter species in which the two species appeared to exchange electrons via interspecies electron transfer. The temperature dependence response of the aggregate conductance was characteristic of the organic metallic-like conductance previously described for the conductive pili of Geobacter sulfurreducens and was inconsistent with electron conduction through minerals. Studies in which aggregates were incubated with high concentrations of potential electron donors demonstrated that the aggregates had no significant capacity for conversion of hydrogen to methane. The aggregates converted formate to methane but at rates too low to account for the rates at which that the aggregates syntrophically metabolized ethanol, an important component of the reactor influent. Geobacter species comprised 25% of 16S rRNA gene sequences recovered from the aggregates, suggesting that Geobacter species may have contributed to some but probably not all of the aggregate conductivity. Microorganisms most closely related to the acetate-utilizing Methanosaeta concilii accounted for more than 90% of the sequences that could be assigned to methane producers, consistent with the poor capacity for hydrogen and formate utilization. These results demonstrate for the first time that methanogenic wastewater aggregates can be electrically conductive and suggest that direct interspecies electron transfer could be an important mechanism for electron exchange in some methanogenic systems.

KW - Archaea

KW - Bacteria

KW - Electron Transport

KW - Methane

KW - Molecular Sequence Data

KW - Sewage

U2 - 10.1128/mBio.00159-11

DO - 10.1128/mBio.00159-11

M3 - Journal article

C2 - 21862629

VL - 2

SP - e00159-11

JO - mBio

JF - mBio

SN - 2161-2129

IS - 4

ER -

Morita M, Malvankar NS, Franks AE, Summers ZM, Giloteaux L, Rotaru AE et al. Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. mBio. 2011;2(4):e00159-11. https://doi.org/10.1128/mBio.00159-11