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Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy

The Favara Grande is a geothermal area located on Pantelleria Island, Italy. The area is characterized high temperatures in the top layer of the soil (60°C), low pH (3–5) and hydrothermal gas emissions mainly composed of carbon dioxide (CO(2)), methane (CH(4)), and hydrogen (H(2)). These geothermal...

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Autores principales: Picone, Nunzia, Blom, Pieter, Wallenius, Anna J., Hogendoorn, Carmen, Mesman, Rob, Cremers, Geert, Gagliano, Antonina L., D’Alessandro, Walter, Quatrini, Paola, Jetten, Mike S. M., Pol, Arjan, Op den Camp, Huub J. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7907005/
https://www.ncbi.nlm.nih.gov/pubmed/33643272
http://dx.doi.org/10.3389/fmicb.2021.637762
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author Picone, Nunzia
Blom, Pieter
Wallenius, Anna J.
Hogendoorn, Carmen
Mesman, Rob
Cremers, Geert
Gagliano, Antonina L.
D’Alessandro, Walter
Quatrini, Paola
Jetten, Mike S. M.
Pol, Arjan
Op den Camp, Huub J. M.
author_facet Picone, Nunzia
Blom, Pieter
Wallenius, Anna J.
Hogendoorn, Carmen
Mesman, Rob
Cremers, Geert
Gagliano, Antonina L.
D’Alessandro, Walter
Quatrini, Paola
Jetten, Mike S. M.
Pol, Arjan
Op den Camp, Huub J. M.
author_sort Picone, Nunzia
collection PubMed
description The Favara Grande is a geothermal area located on Pantelleria Island, Italy. The area is characterized high temperatures in the top layer of the soil (60°C), low pH (3–5) and hydrothermal gas emissions mainly composed of carbon dioxide (CO(2)), methane (CH(4)), and hydrogen (H(2)). These geothermal features may provide a suitable niche for the growth of chemolithotrophic thermoacidophiles, including the lanthanide-dependent methanotrophs of the phylum Verrucomicrobia. In this study, we started enrichment cultures inoculated with soil of the Favara Grande at 50 and 60°C with CH(4) as energy source and medium containing sufficient lanthanides at pH 3 and 5. From these cultures, a verrucomicrobial methanotroph could be isolated via serial dilution and floating filters techniques. The genome of strain AP8 was sequenced and based on phylogenetic analysis we propose to name this new species Methylacidimicrobium thermophilum AP8. The transcriptome data at μ(max) (0.051 ± 0.001 h(−1), doubling time ~14 h) of the new strain showed a high expression of the pmoCAB2 operon encoding the membrane-bound methane monooxygenase and of the gene xoxF1, encoding the lanthanide-dependent methanol dehydrogenase. A second pmoCAB operon and xoxF2 gene were not expressed. The physiology of strain AP8 was further investigated and revealed an optimal growth in a pH range of 3–5 at 50°C, representing the first thermophilic strain of the genus Methylacidimicrobium. Moreover, strain AP8 had a K(S(app)) for methane of 8 ± 1 μM. Beside methane, a type 1b [NiFe] hydrogenase enabled hydrogen oxidation at oxygen concentrations up to 1%. Taken together, our results expand the knowledge on the characteristics and adaptations of verrucomicrobial methanotrophs in hydrothermal environments and add a new thermophilic strain to the genus Methylacidimicrobium.
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spelling pubmed-79070052021-02-27 Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy Picone, Nunzia Blom, Pieter Wallenius, Anna J. Hogendoorn, Carmen Mesman, Rob Cremers, Geert Gagliano, Antonina L. D’Alessandro, Walter Quatrini, Paola Jetten, Mike S. M. Pol, Arjan Op den Camp, Huub J. M. Front Microbiol Microbiology The Favara Grande is a geothermal area located on Pantelleria Island, Italy. The area is characterized high temperatures in the top layer of the soil (60°C), low pH (3–5) and hydrothermal gas emissions mainly composed of carbon dioxide (CO(2)), methane (CH(4)), and hydrogen (H(2)). These geothermal features may provide a suitable niche for the growth of chemolithotrophic thermoacidophiles, including the lanthanide-dependent methanotrophs of the phylum Verrucomicrobia. In this study, we started enrichment cultures inoculated with soil of the Favara Grande at 50 and 60°C with CH(4) as energy source and medium containing sufficient lanthanides at pH 3 and 5. From these cultures, a verrucomicrobial methanotroph could be isolated via serial dilution and floating filters techniques. The genome of strain AP8 was sequenced and based on phylogenetic analysis we propose to name this new species Methylacidimicrobium thermophilum AP8. The transcriptome data at μ(max) (0.051 ± 0.001 h(−1), doubling time ~14 h) of the new strain showed a high expression of the pmoCAB2 operon encoding the membrane-bound methane monooxygenase and of the gene xoxF1, encoding the lanthanide-dependent methanol dehydrogenase. A second pmoCAB operon and xoxF2 gene were not expressed. The physiology of strain AP8 was further investigated and revealed an optimal growth in a pH range of 3–5 at 50°C, representing the first thermophilic strain of the genus Methylacidimicrobium. Moreover, strain AP8 had a K(S(app)) for methane of 8 ± 1 μM. Beside methane, a type 1b [NiFe] hydrogenase enabled hydrogen oxidation at oxygen concentrations up to 1%. Taken together, our results expand the knowledge on the characteristics and adaptations of verrucomicrobial methanotrophs in hydrothermal environments and add a new thermophilic strain to the genus Methylacidimicrobium. Frontiers Media S.A. 2021-02-12 /pmc/articles/PMC7907005/ /pubmed/33643272 http://dx.doi.org/10.3389/fmicb.2021.637762 Text en Copyright © 2021 Picone, Blom, Wallenius, Hogendoorn, Mesman, Cremers, Gagliano, D’Alessandro, Quatrini, Jetten, Pol and Op den Camp. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Picone, Nunzia
Blom, Pieter
Wallenius, Anna J.
Hogendoorn, Carmen
Mesman, Rob
Cremers, Geert
Gagliano, Antonina L.
D’Alessandro, Walter
Quatrini, Paola
Jetten, Mike S. M.
Pol, Arjan
Op den Camp, Huub J. M.
Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy
title Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy
title_full Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy
title_fullStr Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy
title_full_unstemmed Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy
title_short Methylacidimicrobium thermophilum AP8, a Novel Methane- and Hydrogen-Oxidizing Bacterium Isolated From Volcanic Soil on Pantelleria Island, Italy
title_sort methylacidimicrobium thermophilum ap8, a novel methane- and hydrogen-oxidizing bacterium isolated from volcanic soil on pantelleria island, italy
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7907005/
https://www.ncbi.nlm.nih.gov/pubmed/33643272
http://dx.doi.org/10.3389/fmicb.2021.637762
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