Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?

Thermococcales, a major order of hyperthermophilic archaea inhabiting iron- and sulfur-rich anaerobic parts of hydrothermal deep-sea vents, are known to induce the formation of iron phosphates, greigite (Fe3S4) and abundant quantities of pyrite (FeS2), including pyrite spherules. In the present stud...

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Main Authors: Chloé Truong, Sylvain Bernard, Pierre Le Pape, Guillaume Morin, Camille Baya, Pauline Merrot, Aurore Gorlas, François Guyot
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145781/full
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author Chloé Truong
Sylvain Bernard
Pierre Le Pape
Guillaume Morin
Camille Baya
Pauline Merrot
Aurore Gorlas
François Guyot
François Guyot
author_facet Chloé Truong
Sylvain Bernard
Pierre Le Pape
Guillaume Morin
Camille Baya
Pauline Merrot
Aurore Gorlas
François Guyot
François Guyot
author_sort Chloé Truong
collection DOAJ
description Thermococcales, a major order of hyperthermophilic archaea inhabiting iron- and sulfur-rich anaerobic parts of hydrothermal deep-sea vents, are known to induce the formation of iron phosphates, greigite (Fe3S4) and abundant quantities of pyrite (FeS2), including pyrite spherules. In the present study, we report the characterization of the sulfide and phosphate minerals produced in the presence of Thermococcales using X-ray diffraction, synchrotron-based X ray absorption spectroscopy and scanning and transmission electron microscopies. Mixed valence Fe(II)-Fe(III) phosphates are interpreted as resulting from the activity of Thermococcales controlling phosphorus–iron–sulfur dynamics. The pyrite spherules (absent in abiotic control) consist of an assemblage of ultra-small nanocrystals of a few ten nanometers in size, showing coherently diffracting domain sizes of few nanometers. The production of these spherules occurs via a sulfur redox swing from S0 to S–2 and then to S–1, involving a comproportionation of (-II) and (0) oxidation states of sulfur, as supported by S-XANES data. Importantly, these pyrite spherules sequester biogenic organic compounds in small but detectable quantities, possibly making them good biosignatures to be searched for in extreme environments.
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spelling doaj.art-0168ddf19c834a2e9c21cd52adf3291b2023-05-25T04:18:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11457811145781Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?Chloé Truong0Sylvain Bernard1Pierre Le Pape2Guillaume Morin3Camille Baya4Pauline Merrot5Aurore Gorlas6François Guyot7François Guyot8Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceCEA, CNRS, Institute for Integrative Biology of the Cell, Université Paris-Saclay, Gif-sur-Yvette, FranceInstitut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), MNHN, CNRS, IRD, Sorbonne Université, Paris, FranceInstitut Universitaire de France (IUF), Paris, FranceThermococcales, a major order of hyperthermophilic archaea inhabiting iron- and sulfur-rich anaerobic parts of hydrothermal deep-sea vents, are known to induce the formation of iron phosphates, greigite (Fe3S4) and abundant quantities of pyrite (FeS2), including pyrite spherules. In the present study, we report the characterization of the sulfide and phosphate minerals produced in the presence of Thermococcales using X-ray diffraction, synchrotron-based X ray absorption spectroscopy and scanning and transmission electron microscopies. Mixed valence Fe(II)-Fe(III) phosphates are interpreted as resulting from the activity of Thermococcales controlling phosphorus–iron–sulfur dynamics. The pyrite spherules (absent in abiotic control) consist of an assemblage of ultra-small nanocrystals of a few ten nanometers in size, showing coherently diffracting domain sizes of few nanometers. The production of these spherules occurs via a sulfur redox swing from S0 to S–2 and then to S–1, involving a comproportionation of (-II) and (0) oxidation states of sulfur, as supported by S-XANES data. Importantly, these pyrite spherules sequester biogenic organic compounds in small but detectable quantities, possibly making them good biosignatures to be searched for in extreme environments.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145781/fullarchaeabiosignatureshydrothermal ventspyritegreigite
spellingShingle Chloé Truong
Sylvain Bernard
Pierre Le Pape
Guillaume Morin
Camille Baya
Pauline Merrot
Aurore Gorlas
François Guyot
François Guyot
Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?
Frontiers in Microbiology
archaea
biosignatures
hydrothermal vents
pyrite
greigite
title Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?
title_full Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?
title_fullStr Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?
title_full_unstemmed Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?
title_short Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?
title_sort production of carbon containing pyrite spherules induced by hyperthermophilic thermococcales a biosignature
topic archaea
biosignatures
hydrothermal vents
pyrite
greigite
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145781/full
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