Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer

This study describes the potential metabolic pathways by which microbial communities in a serpentinite-influenced aquifer may produce biomass from the products of serpentinization. Serpentinization is a widespread geochemical process, taking place over large regions of the seafloor and at continenta...

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Main Authors: Lauren M. Seyler, William J. Brazelton, Craig McLean, Lindsay I. Putman, Alex Hyer, Michael D. Y. Kubo, Tori Hoehler, Dawn Cardace, Matthew O. Schrenk
Format: Article
Language:English
Published: American Society for Microbiology 2020-03-01
Series:mSystems
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00607-19
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spelling doaj-88a87c9721534794a7cdb0f238ba83062020-11-25T02:43:32ZengAmerican Society for MicrobiologymSystems2379-50772020-03-0152e00607-1910.1128/mSystems.00607-19Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced AquiferLauren M. SeylerWilliam J. BrazeltonCraig McLeanLindsay I. PutmanAlex HyerMichael D. Y. KuboTori HoehlerDawn CardaceMatthew O. SchrenkThis study describes the potential metabolic pathways by which microbial communities in a serpentinite-influenced aquifer may produce biomass from the products of serpentinization. Serpentinization is a widespread geochemical process, taking place over large regions of the seafloor and at continental margins, where ancient seafloor has accreted onto the continents. Because of the difficulty in delineating abiotic and biotic processes in these environments, major questions remain related to microbial contributions to the carbon cycle and physiological adaptation to serpentinite habitats. This research explores multiple mechanisms of carbon fixation and assimilation in serpentinite-hosted microbial communities.Serpentinization is a low-temperature metamorphic process by which ultramafic rock chemically reacts with water. Such reactions provide energy and materials that may be harnessed by chemosynthetic microbial communities at hydrothermal springs and in the subsurface. However, the biogeochemistry mediated by microbial populations that inhabit these environments is understudied and complicated by overlapping biotic and abiotic processes. We applied metagenomics, metatranscriptomics, and untargeted metabolomics techniques to environmental samples taken from the Coast Range Ophiolite Microbial Observatory (CROMO), a subsurface observatory consisting of 12 wells drilled into the ultramafic and serpentinite mélange of the Coast Range Ophiolite in California. Using a combination of DNA and RNA sequence data and mass spectrometry data, we found evidence for several carbon fixation and assimilation strategies, including the Calvin-Benson-Bassham cycle, the reverse tricarboxylic acid cycle, the reductive acetyl coenzyme A (acetyl-CoA) pathway, and methylotrophy, in the microbial communities inhabiting the serpentinite-hosted aquifer. Our data also suggest that the microbial inhabitants of CROMO use products of the serpentinization process, including methane and formate, as carbon sources in a hyperalkaline environment where dissolved inorganic carbon is unavailable.https://doi.org/10.1128/mSystems.00607-19carbon assimilationcarbon fixationformaldehydeformatemethaneserpentinization
collection DOAJ
language English
format Article
sources DOAJ
author Lauren M. Seyler
William J. Brazelton
Craig McLean
Lindsay I. Putman
Alex Hyer
Michael D. Y. Kubo
Tori Hoehler
Dawn Cardace
Matthew O. Schrenk
spellingShingle Lauren M. Seyler
William J. Brazelton
Craig McLean
Lindsay I. Putman
Alex Hyer
Michael D. Y. Kubo
Tori Hoehler
Dawn Cardace
Matthew O. Schrenk
Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer
mSystems
carbon assimilation
carbon fixation
formaldehyde
formate
methane
serpentinization
author_facet Lauren M. Seyler
William J. Brazelton
Craig McLean
Lindsay I. Putman
Alex Hyer
Michael D. Y. Kubo
Tori Hoehler
Dawn Cardace
Matthew O. Schrenk
author_sort Lauren M. Seyler
title Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer
title_short Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer
title_full Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer
title_fullStr Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer
title_full_unstemmed Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer
title_sort carbon assimilation strategies in ultrabasic groundwater: clues from the integrated study of a serpentinization-influenced aquifer
publisher American Society for Microbiology
series mSystems
issn 2379-5077
publishDate 2020-03-01
description This study describes the potential metabolic pathways by which microbial communities in a serpentinite-influenced aquifer may produce biomass from the products of serpentinization. Serpentinization is a widespread geochemical process, taking place over large regions of the seafloor and at continental margins, where ancient seafloor has accreted onto the continents. Because of the difficulty in delineating abiotic and biotic processes in these environments, major questions remain related to microbial contributions to the carbon cycle and physiological adaptation to serpentinite habitats. This research explores multiple mechanisms of carbon fixation and assimilation in serpentinite-hosted microbial communities.Serpentinization is a low-temperature metamorphic process by which ultramafic rock chemically reacts with water. Such reactions provide energy and materials that may be harnessed by chemosynthetic microbial communities at hydrothermal springs and in the subsurface. However, the biogeochemistry mediated by microbial populations that inhabit these environments is understudied and complicated by overlapping biotic and abiotic processes. We applied metagenomics, metatranscriptomics, and untargeted metabolomics techniques to environmental samples taken from the Coast Range Ophiolite Microbial Observatory (CROMO), a subsurface observatory consisting of 12 wells drilled into the ultramafic and serpentinite mélange of the Coast Range Ophiolite in California. Using a combination of DNA and RNA sequence data and mass spectrometry data, we found evidence for several carbon fixation and assimilation strategies, including the Calvin-Benson-Bassham cycle, the reverse tricarboxylic acid cycle, the reductive acetyl coenzyme A (acetyl-CoA) pathway, and methylotrophy, in the microbial communities inhabiting the serpentinite-hosted aquifer. Our data also suggest that the microbial inhabitants of CROMO use products of the serpentinization process, including methane and formate, as carbon sources in a hyperalkaline environment where dissolved inorganic carbon is unavailable.
topic carbon assimilation
carbon fixation
formaldehyde
formate
methane
serpentinization
url https://doi.org/10.1128/mSystems.00607-19
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