Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments

ABSTRACT Coastal sediments are rich in conductive particles, possibly affecting microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermody...

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Autores principales:	Amelia-Elena Rotaru, Federica Calabrese, Hryhoriy Stryhanyuk, Florin Musat, Pravin Malla Shrestha, Hannah Sophia Weber, Oona L. O. Snoeyenbos-West, Per O. J. Hall, Hans H. Richnow, Niculina Musat, Bo Thamdrup
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Desulfuromonadales Geobacter Methanosarcina nanoSIMS activated carbon competitive exclusion Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2ca1e1b350544c6ea3e54e6e8ee5900d
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spelling	oai:doaj.org-article:2ca1e1b350544c6ea3e54e6e8ee5900d2021-11-15T16:00:26ZConductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments10.1128/mBio.00226-182150-7511https://doaj.org/article/2ca1e1b350544c6ea3e54e6e8ee5900d2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00226-18https://doaj.org/toc/2150-7511ABSTRACT Coastal sediments are rich in conductive particles, possibly affecting microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure, and their survival depends on successful partnership. Here, we demonstrate that conductive particles enable the partnership between SAO bacteria (i.e., Geobacter spp.) and methanogens (Methanosarcina spp.) from the coastal sediments of the Bothnian Bay of the Baltic Sea. Baltic methanogenic sediments were rich in conductive minerals, had an apparent isotopic fractionation characteristic of CO2-reductive methanogenesis, and were inhabited by Geobacter and Methanosarcina. As long as conductive particles were delivered, Geobacter and Methanosarcina persisted, whereas exclusion of conductive particles led to the extinction of Geobacter. Baltic Geobacter did not establish a direct electric contact with Methanosarcina, necessitating conductive particles as electrical conduits. Within SAO consortia, Geobacter was an efficient [13C]acetate utilizer, accounting for 82% of the assimilation and 27% of the breakdown of acetate. Geobacter benefits from the association with the methanogen, because in the absence of an electron acceptor it can use Methanosarcina as a terminal electron sink. Consequently, inhibition of methanogenesis constrained the SAO activity of Geobacter as well. A potential benefit for Methanosarcina partnering with Geobacter is that together they competitively exclude acetoclastic methanogens like Methanothrix from an environment rich in conductive particles. Conductive particle-mediated SAO could explain the abundance of acetate oxidizers like Geobacter in the methanogenic zone of sediments where no electron acceptors other than CO2 are available. IMPORTANCE Acetate-oxidizing bacteria are known to thrive in mutualistic consortia in which H2 or formate is shuttled to a methane-producing Archaea partner. Here, we discovered that such bacteria could instead transfer electrons via conductive minerals. Mineral SAO (syntrophic acetate oxidation) could be a vital pathway for CO2-reductive methanogenesis in the environment, especially in sediments rich in conductive minerals. Mineral-facilitated SAO is therefore of potential importance for both iron and methane cycles in sediments and soils. Additionally, our observations imply that agricultural runoff or amendments with conductive chars could trigger a significant increase in methane emissions.Amelia-Elena RotaruFederica CalabreseHryhoriy StryhanyukFlorin MusatPravin Malla ShresthaHannah Sophia WeberOona L. O. Snoeyenbos-WestPer O. J. HallHans H. RichnowNiculina MusatBo ThamdrupAmerican Society for MicrobiologyarticleDesulfuromonadalesGeobacterMethanosarcinananoSIMSactivated carboncompetitive exclusionMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Desulfuromonadales Geobacter Methanosarcina nanoSIMS activated carbon competitive exclusion Microbiology QR1-502
spellingShingle	Desulfuromonadales Geobacter Methanosarcina nanoSIMS activated carbon competitive exclusion Microbiology QR1-502 Amelia-Elena Rotaru Federica Calabrese Hryhoriy Stryhanyuk Florin Musat Pravin Malla Shrestha Hannah Sophia Weber Oona L. O. Snoeyenbos-West Per O. J. Hall Hans H. Richnow Niculina Musat Bo Thamdrup Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments
description	ABSTRACT Coastal sediments are rich in conductive particles, possibly affecting microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure, and their survival depends on successful partnership. Here, we demonstrate that conductive particles enable the partnership between SAO bacteria (i.e., Geobacter spp.) and methanogens (Methanosarcina spp.) from the coastal sediments of the Bothnian Bay of the Baltic Sea. Baltic methanogenic sediments were rich in conductive minerals, had an apparent isotopic fractionation characteristic of CO2-reductive methanogenesis, and were inhabited by Geobacter and Methanosarcina. As long as conductive particles were delivered, Geobacter and Methanosarcina persisted, whereas exclusion of conductive particles led to the extinction of Geobacter. Baltic Geobacter did not establish a direct electric contact with Methanosarcina, necessitating conductive particles as electrical conduits. Within SAO consortia, Geobacter was an efficient [13C]acetate utilizer, accounting for 82% of the assimilation and 27% of the breakdown of acetate. Geobacter benefits from the association with the methanogen, because in the absence of an electron acceptor it can use Methanosarcina as a terminal electron sink. Consequently, inhibition of methanogenesis constrained the SAO activity of Geobacter as well. A potential benefit for Methanosarcina partnering with Geobacter is that together they competitively exclude acetoclastic methanogens like Methanothrix from an environment rich in conductive particles. Conductive particle-mediated SAO could explain the abundance of acetate oxidizers like Geobacter in the methanogenic zone of sediments where no electron acceptors other than CO2 are available. IMPORTANCE Acetate-oxidizing bacteria are known to thrive in mutualistic consortia in which H2 or formate is shuttled to a methane-producing Archaea partner. Here, we discovered that such bacteria could instead transfer electrons via conductive minerals. Mineral SAO (syntrophic acetate oxidation) could be a vital pathway for CO2-reductive methanogenesis in the environment, especially in sediments rich in conductive minerals. Mineral-facilitated SAO is therefore of potential importance for both iron and methane cycles in sediments and soils. Additionally, our observations imply that agricultural runoff or amendments with conductive chars could trigger a significant increase in methane emissions.
format	article
author	Amelia-Elena Rotaru Federica Calabrese Hryhoriy Stryhanyuk Florin Musat Pravin Malla Shrestha Hannah Sophia Weber Oona L. O. Snoeyenbos-West Per O. J. Hall Hans H. Richnow Niculina Musat Bo Thamdrup
author_facet	Amelia-Elena Rotaru Federica Calabrese Hryhoriy Stryhanyuk Florin Musat Pravin Malla Shrestha Hannah Sophia Weber Oona L. O. Snoeyenbos-West Per O. J. Hall Hans H. Richnow Niculina Musat Bo Thamdrup
author_sort	Amelia-Elena Rotaru
title	Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments
title_short	Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments
title_full	Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments
title_fullStr	Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments
title_full_unstemmed	Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments
title_sort	conductive particles enable syntrophic acetate oxidation between <italic toggle="yes">geobacter</italic> and <italic toggle="yes">methanosarcina</italic> from coastal sediments
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/2ca1e1b350544c6ea3e54e6e8ee5900d
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Conductive Particles Enable Syntrophic Acetate Oxidation between <italic toggle="yes">Geobacter</italic> and <italic toggle="yes">Methanosarcina</italic> from Coastal Sediments

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