Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments

<p>Cable bacteria are multicellular, filamentous microorganisms that are capable of transporting electrons over centimeter-scale distances. Although recently discovered, these bacteria appear to be widely present in the seafloor, and when active they exert a strong imprint on the local geochem...

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Main Authors: N. M. J. Geerlings, E.-M. Zetsche, S. Hidalgo-Martinez, J. J. Middelburg, F. J. R. Meysman
Format: Article
Language:English
Published: Copernicus Publications 2019-02-01
Series:Biogeosciences
Online Access:https://www.biogeosciences.net/16/811/2019/bg-16-811-2019.pdf
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author N. M. J. Geerlings
E.-M. Zetsche
E.-M. Zetsche
S. Hidalgo-Martinez
J. J. Middelburg
F. J. R. Meysman
F. J. R. Meysman
author_facet N. M. J. Geerlings
E.-M. Zetsche
E.-M. Zetsche
S. Hidalgo-Martinez
J. J. Middelburg
F. J. R. Meysman
F. J. R. Meysman
author_sort N. M. J. Geerlings
collection DOAJ
description <p>Cable bacteria are multicellular, filamentous microorganisms that are capable of transporting electrons over centimeter-scale distances. Although recently discovered, these bacteria appear to be widely present in the seafloor, and when active they exert a strong imprint on the local geochemistry. In particular, their electrogenic metabolism induces unusually strong pH excursions in aquatic sediments, which induces considerable mineral dissolution, and subsequent mineral reprecipitation. However, at present, it is unknown whether and how cable bacteria play an active or direct role in the mineral reprecipitation process. To this end we present an explorative study of the formation of sedimentary minerals in and near filamentous cable bacteria using a combined approach of electron microscopy and spectroscopic techniques. Our observations reveal the formation of polyphosphate granules within the cells and two different types of biomineral formation directly associated with multicellular filaments of these cable bacteria: (i) the attachment and incorporation of clay particles in a coating surrounding the bacteria and (ii) encrustation of the cell envelope by iron minerals. These findings suggest a complex interaction between cable bacteria and the surrounding sediment matrix, and a substantial imprint of the electrogenic metabolism on mineral diagenesis and sedimentary biogeochemical cycling. In particular, the encrustation process leaves many open questions for further research. For example, we hypothesize that the complete encrustation of filaments might create a diffusion barrier and negatively impact the metabolism of the cable bacteria.</p>
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spelling doaj.art-29226b72cb334933a1bbd873d7afff5c2022-12-21T20:36:41ZengCopernicus PublicationsBiogeosciences1726-41701726-41892019-02-011681182910.5194/bg-16-811-2019Mineral formation induced by cable bacteria performing long-distance electron transport in marine sedimentsN. M. J. Geerlings0E.-M. Zetsche1E.-M. Zetsche2S. Hidalgo-Martinez3J. J. Middelburg4F. J. R. Meysman5F. J. R. Meysman6Department of Earth Sciences, Utrecht University, Princetonplein 8a, 3584 CB Utrecht, the NetherlandsDepartment of Marine Sciences, University of Gothenburg, Carl Skottsberg gata 22B, 41319 Gothenburg, SwedenDepartment of Estuarine and Delta Systems, Royal Netherlands Institute for Sea Research, Utrecht University, Korringaweg 7, 4401 NT Yerseke, the NetherlandsDepartment of Biology, Ecosystem Management Research Group, Universiteit Antwerpen, Universiteitsplein 1, 2160 Antwerp, BelgiumDepartment of Earth Sciences, Utrecht University, Princetonplein 8a, 3584 CB Utrecht, the NetherlandsDepartment of Biology, Ecosystem Management Research Group, Universiteit Antwerpen, Universiteitsplein 1, 2160 Antwerp, BelgiumDepartment of Biotechnology, Delft University of Technology, Van der Maasweg 9, 2629 HZ Delft, the Netherlands<p>Cable bacteria are multicellular, filamentous microorganisms that are capable of transporting electrons over centimeter-scale distances. Although recently discovered, these bacteria appear to be widely present in the seafloor, and when active they exert a strong imprint on the local geochemistry. In particular, their electrogenic metabolism induces unusually strong pH excursions in aquatic sediments, which induces considerable mineral dissolution, and subsequent mineral reprecipitation. However, at present, it is unknown whether and how cable bacteria play an active or direct role in the mineral reprecipitation process. To this end we present an explorative study of the formation of sedimentary minerals in and near filamentous cable bacteria using a combined approach of electron microscopy and spectroscopic techniques. Our observations reveal the formation of polyphosphate granules within the cells and two different types of biomineral formation directly associated with multicellular filaments of these cable bacteria: (i) the attachment and incorporation of clay particles in a coating surrounding the bacteria and (ii) encrustation of the cell envelope by iron minerals. These findings suggest a complex interaction between cable bacteria and the surrounding sediment matrix, and a substantial imprint of the electrogenic metabolism on mineral diagenesis and sedimentary biogeochemical cycling. In particular, the encrustation process leaves many open questions for further research. For example, we hypothesize that the complete encrustation of filaments might create a diffusion barrier and negatively impact the metabolism of the cable bacteria.</p>https://www.biogeosciences.net/16/811/2019/bg-16-811-2019.pdf
spellingShingle N. M. J. Geerlings
E.-M. Zetsche
E.-M. Zetsche
S. Hidalgo-Martinez
J. J. Middelburg
F. J. R. Meysman
F. J. R. Meysman
Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments
Biogeosciences
title Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments
title_full Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments
title_fullStr Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments
title_full_unstemmed Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments
title_short Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments
title_sort mineral formation induced by cable bacteria performing long distance electron transport in marine sediments
url https://www.biogeosciences.net/16/811/2019/bg-16-811-2019.pdf
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