Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals
The genus Carboxydocella forms a deeply branching family in the class Clostridia and is currently represented by three physiologically diverse species of thermophilic prokaryotes. The type strain of the type species, Carboxydocella thermautotrophica 41T, is an obligate chemolithoautotroph growing ex...
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ftdoajarticles:oai:doaj.org/article:8e9f21f5ebf04cb28d4ef08f0ae978d6 2023-05-15T16:59:03+02:00 Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals Stepan V. Toshchakov Alexander V. Lebedinsky Tatyana G. Sokolova Daria G. Zavarzina Alexei A. Korzhenkov Alina V. Teplyuk Natalia I. Chistyakova Vyacheslav S. Rusakov Elizaveta A. Bonch-Osmolovskaya Ilya V. Kublanov Sergey N. Gavrilov 2018-08-01T00:00:00Z https://doi.org/10.3389/fmicb.2018.01759 https://doaj.org/article/8e9f21f5ebf04cb28d4ef08f0ae978d6 EN eng Frontiers Media S.A. https://www.frontiersin.org/article/10.3389/fmicb.2018.01759/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2018.01759 https://doaj.org/article/8e9f21f5ebf04cb28d4ef08f0ae978d6 Frontiers in Microbiology, Vol 9 (2018) Carboxydocella thermophile Kamchatka hot springs genomics hydrogenogenic carboxydotrophy Fe(III) reduction Microbiology QR1-502 article 2018 ftdoajarticles https://doi.org/10.3389/fmicb.2018.01759 2022-12-31T06:44:07Z The genus Carboxydocella forms a deeply branching family in the class Clostridia and is currently represented by three physiologically diverse species of thermophilic prokaryotes. The type strain of the type species, Carboxydocella thermautotrophica 41T, is an obligate chemolithoautotroph growing exclusively by hydrogenogenic CO oxidation. Another strain, isolated from a hot spring at Uzon caldera, Kamchatka in the course of this work, is capable of coupling carboxydotrophy and dissimilatory reduction of Fe(III) from oxic and phyllosilicate minerals. The processes of carboxydotrophy and Fe(III) reduction appeared to be interdependent in this strain. The genomes of both isolates were sequenced, assembled into single chromosome sequences (for strain 41T a plasmid sequence was also assembled) and analyzed. Genome analysis revealed that each of the two strains possessed six genes encoding diverse Ni,Fe-containing CO dehydrogenases (maximum reported in complete prokaryotic genomes), indicating crucial role of carbon monoxide in C. thermautotrophica metabolism. Both strains possessed a set of 30 multiheme c-type cytochromes, but only the newly isolated Fe-reducing strain 019 had one extra gene of a 17-heme cytochrome, which is proposed to represent a novel determinant of dissimilatory iron reduction in prokaryotes. Mössbauer studies revealed that strain 019 induced reductive transformation of the abundant ferric/ferrous-mica mineral glauconite to siderite during carboxydotrophic growth. Reconstruction of the C. thermautotrophica strains energy metabolism is the first comprehensive genome analysis of a representative of the deep phylogenetic branch Clostridia Incertae Sedis, family V. Our data provide insights into energy metabolism of C. thermautotrophica with an emphasis on its ecological implications. Article in Journal/Newspaper Kamchatka Directory of Open Access Journals: DOAJ Articles Frontiers in Microbiology 9 |
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Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
Carboxydocella thermophile Kamchatka hot springs genomics hydrogenogenic carboxydotrophy Fe(III) reduction Microbiology QR1-502 |
spellingShingle |
Carboxydocella thermophile Kamchatka hot springs genomics hydrogenogenic carboxydotrophy Fe(III) reduction Microbiology QR1-502 Stepan V. Toshchakov Alexander V. Lebedinsky Tatyana G. Sokolova Daria G. Zavarzina Alexei A. Korzhenkov Alina V. Teplyuk Natalia I. Chistyakova Vyacheslav S. Rusakov Elizaveta A. Bonch-Osmolovskaya Ilya V. Kublanov Sergey N. Gavrilov Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals |
topic_facet |
Carboxydocella thermophile Kamchatka hot springs genomics hydrogenogenic carboxydotrophy Fe(III) reduction Microbiology QR1-502 |
description |
The genus Carboxydocella forms a deeply branching family in the class Clostridia and is currently represented by three physiologically diverse species of thermophilic prokaryotes. The type strain of the type species, Carboxydocella thermautotrophica 41T, is an obligate chemolithoautotroph growing exclusively by hydrogenogenic CO oxidation. Another strain, isolated from a hot spring at Uzon caldera, Kamchatka in the course of this work, is capable of coupling carboxydotrophy and dissimilatory reduction of Fe(III) from oxic and phyllosilicate minerals. The processes of carboxydotrophy and Fe(III) reduction appeared to be interdependent in this strain. The genomes of both isolates were sequenced, assembled into single chromosome sequences (for strain 41T a plasmid sequence was also assembled) and analyzed. Genome analysis revealed that each of the two strains possessed six genes encoding diverse Ni,Fe-containing CO dehydrogenases (maximum reported in complete prokaryotic genomes), indicating crucial role of carbon monoxide in C. thermautotrophica metabolism. Both strains possessed a set of 30 multiheme c-type cytochromes, but only the newly isolated Fe-reducing strain 019 had one extra gene of a 17-heme cytochrome, which is proposed to represent a novel determinant of dissimilatory iron reduction in prokaryotes. Mössbauer studies revealed that strain 019 induced reductive transformation of the abundant ferric/ferrous-mica mineral glauconite to siderite during carboxydotrophic growth. Reconstruction of the C. thermautotrophica strains energy metabolism is the first comprehensive genome analysis of a representative of the deep phylogenetic branch Clostridia Incertae Sedis, family V. Our data provide insights into energy metabolism of C. thermautotrophica with an emphasis on its ecological implications. |
format |
Article in Journal/Newspaper |
author |
Stepan V. Toshchakov Alexander V. Lebedinsky Tatyana G. Sokolova Daria G. Zavarzina Alexei A. Korzhenkov Alina V. Teplyuk Natalia I. Chistyakova Vyacheslav S. Rusakov Elizaveta A. Bonch-Osmolovskaya Ilya V. Kublanov Sergey N. Gavrilov |
author_facet |
Stepan V. Toshchakov Alexander V. Lebedinsky Tatyana G. Sokolova Daria G. Zavarzina Alexei A. Korzhenkov Alina V. Teplyuk Natalia I. Chistyakova Vyacheslav S. Rusakov Elizaveta A. Bonch-Osmolovskaya Ilya V. Kublanov Sergey N. Gavrilov |
author_sort |
Stepan V. Toshchakov |
title |
Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals |
title_short |
Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals |
title_full |
Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals |
title_fullStr |
Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals |
title_full_unstemmed |
Genomic Insights Into Energy Metabolism of Carboxydocella thermautotrophica Coupling Hydrogenogenic CO Oxidation With the Reduction of Fe(III) Minerals |
title_sort |
genomic insights into energy metabolism of carboxydocella thermautotrophica coupling hydrogenogenic co oxidation with the reduction of fe(iii) minerals |
publisher |
Frontiers Media S.A. |
publishDate |
2018 |
url |
https://doi.org/10.3389/fmicb.2018.01759 https://doaj.org/article/8e9f21f5ebf04cb28d4ef08f0ae978d6 |
genre |
Kamchatka |
genre_facet |
Kamchatka |
op_source |
Frontiers in Microbiology, Vol 9 (2018) |
op_relation |
https://www.frontiersin.org/article/10.3389/fmicb.2018.01759/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2018.01759 https://doaj.org/article/8e9f21f5ebf04cb28d4ef08f0ae978d6 |
op_doi |
https://doi.org/10.3389/fmicb.2018.01759 |
container_title |
Frontiers in Microbiology |
container_volume |
9 |
_version_ |
1766051221059141632 |