<i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt

The Iberian Pyrite Belt (IPB) is one of the largest deposits of sulphidic minerals on Earth. Río Tinto raises from its core, presenting low a pH and high metal concentration. Several drilling cores were extracted from the IPB’s subsurface, and strain T2.3D-1.1 was isolated from a core at 121.8 m dep...

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Main Authors: Guillermo Mateos, Adrián Martínez Bonilla, Sofía de Francisco de Polanco, José M. Martínez, Cristina Escudero, Nuria Rodríguez, Irene Sánchez-Andrea, Ricardo Amils
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/10/8/1585
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author Guillermo Mateos
Adrián Martínez Bonilla
Sofía de Francisco de Polanco
José M. Martínez
Cristina Escudero
Nuria Rodríguez
Irene Sánchez-Andrea
Ricardo Amils
author_facet Guillermo Mateos
Adrián Martínez Bonilla
Sofía de Francisco de Polanco
José M. Martínez
Cristina Escudero
Nuria Rodríguez
Irene Sánchez-Andrea
Ricardo Amils
author_sort Guillermo Mateos
collection DOAJ
description The Iberian Pyrite Belt (IPB) is one of the largest deposits of sulphidic minerals on Earth. Río Tinto raises from its core, presenting low a pH and high metal concentration. Several drilling cores were extracted from the IPB’s subsurface, and strain T2.3D-1.1 was isolated from a core at 121.8 m depth. We aimed to characterize this subterranean microorganism, revealing its phylogenomic affiliation (Average Nucleotide Identity, digital DNA-DNA Hybridization) and inferring its physiology through genome annotation, backed with physiological experiments to explore its relationship with the Fe biogeochemical cycle. Results determined that the isolate belongs to the <i>Shewanella putrefaciens</i> (with ANI 99.25 with <i>S. putrefaciens</i> CN-32). Its genome harbours the necessary genes, including <i>omc</i>A <i>mtr</i>CAB, to perform the Extracellular Electron Transfer (EET) and reduce acceptors such as Fe<sup>3+</sup>, <i>nap</i>AB to reduce NO<sub>3</sub><sup>−</sup> to NO<sub>2</sub><sup>−</sup>, <i>hyd</i>AB to produce H<sub>2</sub> and genes <i>sir</i>A, <i>phs</i>ABC and <i>ttr</i>ABC to reduce SO<sub>3</sub><sup>2−</sup>, S<sub>2</sub>O<sub>3</sub><sup>2−</sup> and S<sub>4</sub>O<sub>6</sub><sup>2−</sup>, respectively. A full CRISPR-Cas 1F type system was found as well. <i>S. putrefaciens</i> T2.3D-1.1 can reduce Fe<sup>3+</sup> and promote the oxidation of Fe<sup>2+</sup> in the presence of NO<sub>3</sub><sup>−</sup> under anaerobic conditions. Production of H<sub>2</sub> has been observed under anaerobic conditions with lactate or pyruvate as the electron donor and fumarate as the electron acceptor. Besides Fe<sup>3+</sup> and NO<sub>3</sub><sup>−</sup>, the isolate also grows with Dimethyl Sulfoxide and Trimethyl N-oxide, S<sub>4</sub>O<sub>6</sub><sup>2−</sup> and S<sub>2</sub>O<sub>3</sub><sup>2−</sup> as electron acceptors. It tolerates different concentrations of heavy metals such as 7.5 mM of Pb, 5 mM of Cr and Cu and 1 mM of Cd, Co, Ni and Zn. This array of traits suggests that <i>S. putrefaciens</i> T2.3D-1.1 could have an important role within the Iberian Pyrite Belt subsurface participating in the iron cycle, through the dissolution of iron minerals and therefore contributing to generate the extreme conditions detected in the Río Tinto basin.
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spelling doaj.art-80c6f4fc8e084a9bb909b6ad1aba49162023-12-02T00:02:35ZengMDPI AGMicroorganisms2076-26072022-08-01108158510.3390/microorganisms10081585<i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite BeltGuillermo Mateos0Adrián Martínez Bonilla1Sofía de Francisco de Polanco2José M. Martínez3Cristina Escudero4Nuria Rodríguez5Irene Sánchez-Andrea6Ricardo Amils7Centro de Biología Molecular Severo Ochoa, Nicolás Cabrera 1, 28049 Madrid, SpainCentro de Biología Molecular Severo Ochoa, Nicolás Cabrera 1, 28049 Madrid, SpainCentro de Investigaciones Biológicas, Ramiro de Maeztu 9, 28040 Madrid, SpainCentro de Biología Molecular Severo Ochoa, Nicolás Cabrera 1, 28049 Madrid, SpainCentro de Astrobiología (CAB-INTA), 28850 Torrejón de Ardoz, SpainCentro de Biología Molecular Severo Ochoa, Nicolás Cabrera 1, 28049 Madrid, SpainLaboratory of Microbiology, Wageningen University & Research, Stippeneng, 46708 Wageningen, The NetherlandsCentro de Biología Molecular Severo Ochoa, Nicolás Cabrera 1, 28049 Madrid, SpainThe Iberian Pyrite Belt (IPB) is one of the largest deposits of sulphidic minerals on Earth. Río Tinto raises from its core, presenting low a pH and high metal concentration. Several drilling cores were extracted from the IPB’s subsurface, and strain T2.3D-1.1 was isolated from a core at 121.8 m depth. We aimed to characterize this subterranean microorganism, revealing its phylogenomic affiliation (Average Nucleotide Identity, digital DNA-DNA Hybridization) and inferring its physiology through genome annotation, backed with physiological experiments to explore its relationship with the Fe biogeochemical cycle. Results determined that the isolate belongs to the <i>Shewanella putrefaciens</i> (with ANI 99.25 with <i>S. putrefaciens</i> CN-32). Its genome harbours the necessary genes, including <i>omc</i>A <i>mtr</i>CAB, to perform the Extracellular Electron Transfer (EET) and reduce acceptors such as Fe<sup>3+</sup>, <i>nap</i>AB to reduce NO<sub>3</sub><sup>−</sup> to NO<sub>2</sub><sup>−</sup>, <i>hyd</i>AB to produce H<sub>2</sub> and genes <i>sir</i>A, <i>phs</i>ABC and <i>ttr</i>ABC to reduce SO<sub>3</sub><sup>2−</sup>, S<sub>2</sub>O<sub>3</sub><sup>2−</sup> and S<sub>4</sub>O<sub>6</sub><sup>2−</sup>, respectively. A full CRISPR-Cas 1F type system was found as well. <i>S. putrefaciens</i> T2.3D-1.1 can reduce Fe<sup>3+</sup> and promote the oxidation of Fe<sup>2+</sup> in the presence of NO<sub>3</sub><sup>−</sup> under anaerobic conditions. Production of H<sub>2</sub> has been observed under anaerobic conditions with lactate or pyruvate as the electron donor and fumarate as the electron acceptor. Besides Fe<sup>3+</sup> and NO<sub>3</sub><sup>−</sup>, the isolate also grows with Dimethyl Sulfoxide and Trimethyl N-oxide, S<sub>4</sub>O<sub>6</sub><sup>2−</sup> and S<sub>2</sub>O<sub>3</sub><sup>2−</sup> as electron acceptors. It tolerates different concentrations of heavy metals such as 7.5 mM of Pb, 5 mM of Cr and Cu and 1 mM of Cd, Co, Ni and Zn. This array of traits suggests that <i>S. putrefaciens</i> T2.3D-1.1 could have an important role within the Iberian Pyrite Belt subsurface participating in the iron cycle, through the dissolution of iron minerals and therefore contributing to generate the extreme conditions detected in the Río Tinto basin.https://www.mdpi.com/2076-2607/10/8/1585<i>Shewanella putrefaciens</i>deep subsurfacehydrogenironNDFO
spellingShingle Guillermo Mateos
Adrián Martínez Bonilla
Sofía de Francisco de Polanco
José M. Martínez
Cristina Escudero
Nuria Rodríguez
Irene Sánchez-Andrea
Ricardo Amils
<i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt
Microorganisms
<i>Shewanella putrefaciens</i>
deep subsurface
hydrogen
iron
NDFO
title <i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt
title_full <i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt
title_fullStr <i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt
title_full_unstemmed <i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt
title_short <i>Shewanella</i> sp. T2.3D-1.1 a Novel Microorganism Sustaining the Iron Cycle in the Deep Subsurface of the Iberian Pyrite Belt
title_sort i shewanella i sp t2 3d 1 1 a novel microorganism sustaining the iron cycle in the deep subsurface of the iberian pyrite belt
topic <i>Shewanella putrefaciens</i>
deep subsurface
hydrogen
iron
NDFO
url https://www.mdpi.com/2076-2607/10/8/1585
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