Coupled C, H, N, S and Fe biogeochemical cycles operating in the continental deep subsurface of the Iberian Pyrite Belt

Ricardo Amils; Fernando Puente-Sánchez; Monike Oggerin; Nuria Rodríguez; Monica Sanchez Roman; Víctor Parro; David Fernández-Remolar

doi:10.1111/1462-2920.16291

Coupled C, H, N, S and Fe biogeochemical cycles operating in the continental deep subsurface of the Iberian Pyrite Belt

Ricardo Amils, Fernando Puente-Sánchez, Monike Oggerin, Nuria Rodríguez, Monica Sanchez Roman, Víctor Parro, David Fernández-Remolar

Geology and Geochemistry

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Microbial activity is a major contributor to the biogeochemical cycles that make up the life support system of planet Earth. A 613 m deep geomicrobiological perforation and a systematic multi-analytical characterization revealed an unexpected diversity associated with the rock matrix microbiome that operates in the subsurface of the Iberian Pyrite Belt (IPB). Members of 1 class and 16 genera were deemed the most representative microorganisms of the IPB deep subsurface and selected for a deeper analysis. The use of fluorescence in situ hybridization allowed not only the identification of microorganisms but also the detection of novel activities in the subsurface such as anaerobic ammonium oxidation (ANAMMOX) and anaerobic methane oxidation, the co-occurrence of microorganisms able to maintain complementary metabolic activities and the existence of biofilms. The use of enrichment cultures sensed the presence of five different complementary metabolic activities along the length of the borehole and isolated 29 bacterial species. Genomic analysis of nine isolates identified the genes involved in the complete operation of the light-independent coupled C, H, N, S and Fe biogeochemical cycles. This study revealed the importance of nitrate reduction microorganisms in the oxidation of iron in the anoxic conditions existing in the subsurface of the IPB.

Original language	English
Pages (from-to)	428-453
Number of pages	16
Journal	Environmental Microbiology
Volume	25
Issue number	2
Early online date	1 Dec 2022
DOIs	https://doi.org/10.1111/1462-2920.16291
Publication status	Published - Feb 2023

Funding

The authors thank J. P. Fernández‐Rodríguez, J. A. Rodríguez‐Manfredi, F. López de Saro, E. Omoregie, M. Fernández‐Algar, M. Postigo, P. Cruz‐Gil, Y. Blanco, M. Fernández Sampedro, M. Martín (from the Centro de Astrobiología) and J. M. Martínez (U. Autónoma de Madrid), D. Gómez‐Ortiz (U. Rey Juan Carlos), L. Loiselle (Australian National U.), the Optical and Confocal Microscopy Service (CBMSO), and the Unit of Elemental Analysis (Sidi, U. Autónoma de Madrid) for their collaboration in different tasks of the project, and R. Samalot for the English correction of the manuscript. The authors thank C. Primo and A. Primo (Hotel Vázquez Diaz, Nerva, Spain), different members of the Fundación Río Tinto and the Museo Minero de Riotinto “Ernest Lluch” for their valuable collaboration in different aspects of the drilling part of the project. This work has been supported by the ERC Advance Grant #250‐350 “Iberian Pyrite Belt Subsurface Life Detection” (IPBSL). FP7 Ideas: European Research Council, Grant/Award Number: ERC Advanced Grant #250‐350 Funding information The authors thank J. P. Fernández-Rodríguez, J. A. Rodríguez-Manfredi, F. López de Saro, E. Omoregie, M. Fernández-Algar, M. Postigo, P. Cruz-Gil, Y. Blanco, M. Fernández Sampedro, M. Martín (from the Centro de Astrobiología) and J. M. Martínez (U. Autónoma de Madrid), D. Gómez-Ortiz (U. Rey Juan Carlos), L. Loiselle (Australian National U.), the Optical and Confocal Microscopy Service (CBMSO), and the Unit of Elemental Analysis (Sidi, U. Autónoma de Madrid) for their collaboration in different tasks of the project, and R. Samalot for the English correction of the manuscript. The authors thank C. Primo and A. Primo (Hotel Vázquez Diaz, Nerva, Spain), different members of the Fundación Río Tinto and the Museo Minero de Riotinto “Ernest Lluch” for their valuable collaboration in different aspects of the drilling part of the project. This work has been supported by the ERC Advance Grant #250-350 “Iberian Pyrite Belt Subsurface Life Detection” (IPBSL).

Funders	Funder number
Centro de Astrobiología
Fundación Río Tinto
U. Autónoma de Madrid
European Research Council	250‐350

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title = "Coupled C, H, N, S and Fe biogeochemical cycles operating in the continental deep subsurface of the Iberian Pyrite Belt",

abstract = "Microbial activity is a major contributor to the biogeochemical cycles that make up the life support system of planet Earth. A 613 m deep geomicrobiological perforation and a systematic multi-analytical characterization revealed an unexpected diversity associated with the rock matrix microbiome that operates in the subsurface of the Iberian Pyrite Belt (IPB). Members of 1 class and 16 genera were deemed the most representative microorganisms of the IPB deep subsurface and selected for a deeper analysis. The use of fluorescence in situ hybridization allowed not only the identification of microorganisms but also the detection of novel activities in the subsurface such as anaerobic ammonium oxidation (ANAMMOX) and anaerobic methane oxidation, the co-occurrence of microorganisms able to maintain complementary metabolic activities and the existence of biofilms. The use of enrichment cultures sensed the presence of five different complementary metabolic activities along the length of the borehole and isolated 29 bacterial species. Genomic analysis of nine isolates identified the genes involved in the complete operation of the light-independent coupled C, H, N, S and Fe biogeochemical cycles. This study revealed the importance of nitrate reduction microorganisms in the oxidation of iron in the anoxic conditions existing in the subsurface of the IPB.",

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AU - Amils, Ricardo

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AU - Oggerin, Monike

AU - Rodríguez, Nuria

AU - Sanchez Roman, Monica

AU - Parro, Víctor

AU - Fernández-Remolar, David

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N2 - Microbial activity is a major contributor to the biogeochemical cycles that make up the life support system of planet Earth. A 613 m deep geomicrobiological perforation and a systematic multi-analytical characterization revealed an unexpected diversity associated with the rock matrix microbiome that operates in the subsurface of the Iberian Pyrite Belt (IPB). Members of 1 class and 16 genera were deemed the most representative microorganisms of the IPB deep subsurface and selected for a deeper analysis. The use of fluorescence in situ hybridization allowed not only the identification of microorganisms but also the detection of novel activities in the subsurface such as anaerobic ammonium oxidation (ANAMMOX) and anaerobic methane oxidation, the co-occurrence of microorganisms able to maintain complementary metabolic activities and the existence of biofilms. The use of enrichment cultures sensed the presence of five different complementary metabolic activities along the length of the borehole and isolated 29 bacterial species. Genomic analysis of nine isolates identified the genes involved in the complete operation of the light-independent coupled C, H, N, S and Fe biogeochemical cycles. This study revealed the importance of nitrate reduction microorganisms in the oxidation of iron in the anoxic conditions existing in the subsurface of the IPB.

AB - Microbial activity is a major contributor to the biogeochemical cycles that make up the life support system of planet Earth. A 613 m deep geomicrobiological perforation and a systematic multi-analytical characterization revealed an unexpected diversity associated with the rock matrix microbiome that operates in the subsurface of the Iberian Pyrite Belt (IPB). Members of 1 class and 16 genera were deemed the most representative microorganisms of the IPB deep subsurface and selected for a deeper analysis. The use of fluorescence in situ hybridization allowed not only the identification of microorganisms but also the detection of novel activities in the subsurface such as anaerobic ammonium oxidation (ANAMMOX) and anaerobic methane oxidation, the co-occurrence of microorganisms able to maintain complementary metabolic activities and the existence of biofilms. The use of enrichment cultures sensed the presence of five different complementary metabolic activities along the length of the borehole and isolated 29 bacterial species. Genomic analysis of nine isolates identified the genes involved in the complete operation of the light-independent coupled C, H, N, S and Fe biogeochemical cycles. This study revealed the importance of nitrate reduction microorganisms in the oxidation of iron in the anoxic conditions existing in the subsurface of the IPB.

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DO - 10.1111/1462-2920.16291

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JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 2

ER -

Coupled C, H, N, S and Fe biogeochemical cycles operating in the continental deep subsurface of the Iberian Pyrite Belt

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