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Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin
Melioribacter roseus, a representative of recently proposed Ignavibacteriae phylum, is a metabolically versatile thermophilic bacterium, inhabiting subsurface biosphere of the West-Siberian megabasin and capable of growing on various substrates and electron acceptors. Genomic analysis followed by in...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5492636/ https://www.ncbi.nlm.nih.gov/pubmed/28713355 http://dx.doi.org/10.3389/fmicb.2017.01228 |
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author | Gavrilov, Sergey Podosokorskaya, Olga Alexeev, Dmitry Merkel, Alexander Khomyakova, Maria Muntyan, Maria Altukhov, Ilya Butenko, Ivan Bonch-Osmolovskaya, Elizaveta Govorun, Vadim Kublanov, Ilya |
author_facet | Gavrilov, Sergey Podosokorskaya, Olga Alexeev, Dmitry Merkel, Alexander Khomyakova, Maria Muntyan, Maria Altukhov, Ilya Butenko, Ivan Bonch-Osmolovskaya, Elizaveta Govorun, Vadim Kublanov, Ilya |
author_sort | Gavrilov, Sergey |
collection | PubMed |
description | Melioribacter roseus, a representative of recently proposed Ignavibacteriae phylum, is a metabolically versatile thermophilic bacterium, inhabiting subsurface biosphere of the West-Siberian megabasin and capable of growing on various substrates and electron acceptors. Genomic analysis followed by inhibitor studies and membrane potential measurements of aerobically grown M. roseus cells revealed the activity of aerobic respiratory electron transfer chain comprised of respiratory complexes I and IV, and an alternative complex III. Phylogeny reconstruction revealed that oxygen reductases belonged to atypical cc(o/b)o(3)-type and canonical cbb(3)–type cytochrome oxidases. Also, two molybdoenzymes of M. roseus were affiliated either with Ttr or Psr/Phs clades, but not with typical respiratory arsenate reductases of the Arr clade. Expression profiling, both at transcripts and protein level, allowed us to assign the role of the terminal respiratory oxidase under atmospheric oxygen concentration for the cc(o/b)o(3) cytochrome oxidase, previously proposed to serve for oxygen detoxification only. Transcriptomic analysis revealed the involvement of both molybdoenzymes of M. roseus in As(V) respiration, yet differences in the genomic context of their gene clusters allow to hypothesize about their distinct roles in arsenate metabolism with the ‘Psr/Phs’-type molybdoenzyme being the most probable candidate respiratory arsenate reductase. Basing on multi-omics data, the pathways for aerobic and arsenate respiration were proposed. Our results start to bridge the vigorously increasing gap between homology-based predictions and experimentally verified metabolic processes, what is especially important for understudied microorganisms of novel lineages from deep subsurface environments of Eurasia, which remained separated from the rest of the biosphere for several geological periods. |
format | Online Article Text |
id | pubmed-5492636 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-54926362017-07-14 Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin Gavrilov, Sergey Podosokorskaya, Olga Alexeev, Dmitry Merkel, Alexander Khomyakova, Maria Muntyan, Maria Altukhov, Ilya Butenko, Ivan Bonch-Osmolovskaya, Elizaveta Govorun, Vadim Kublanov, Ilya Front Microbiol Microbiology Melioribacter roseus, a representative of recently proposed Ignavibacteriae phylum, is a metabolically versatile thermophilic bacterium, inhabiting subsurface biosphere of the West-Siberian megabasin and capable of growing on various substrates and electron acceptors. Genomic analysis followed by inhibitor studies and membrane potential measurements of aerobically grown M. roseus cells revealed the activity of aerobic respiratory electron transfer chain comprised of respiratory complexes I and IV, and an alternative complex III. Phylogeny reconstruction revealed that oxygen reductases belonged to atypical cc(o/b)o(3)-type and canonical cbb(3)–type cytochrome oxidases. Also, two molybdoenzymes of M. roseus were affiliated either with Ttr or Psr/Phs clades, but not with typical respiratory arsenate reductases of the Arr clade. Expression profiling, both at transcripts and protein level, allowed us to assign the role of the terminal respiratory oxidase under atmospheric oxygen concentration for the cc(o/b)o(3) cytochrome oxidase, previously proposed to serve for oxygen detoxification only. Transcriptomic analysis revealed the involvement of both molybdoenzymes of M. roseus in As(V) respiration, yet differences in the genomic context of their gene clusters allow to hypothesize about their distinct roles in arsenate metabolism with the ‘Psr/Phs’-type molybdoenzyme being the most probable candidate respiratory arsenate reductase. Basing on multi-omics data, the pathways for aerobic and arsenate respiration were proposed. Our results start to bridge the vigorously increasing gap between homology-based predictions and experimentally verified metabolic processes, what is especially important for understudied microorganisms of novel lineages from deep subsurface environments of Eurasia, which remained separated from the rest of the biosphere for several geological periods. Frontiers Media S.A. 2017-06-30 /pmc/articles/PMC5492636/ /pubmed/28713355 http://dx.doi.org/10.3389/fmicb.2017.01228 Text en Copyright © 2017 Gavrilov, Podosokorskaya, Alexeev, Merkel, Khomyakova, Muntyan, Altukhov, Butenko, Bonch-Osmolovskaya, Govorun and Kublanov. 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) or licensor 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 Gavrilov, Sergey Podosokorskaya, Olga Alexeev, Dmitry Merkel, Alexander Khomyakova, Maria Muntyan, Maria Altukhov, Ilya Butenko, Ivan Bonch-Osmolovskaya, Elizaveta Govorun, Vadim Kublanov, Ilya Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin |
title | Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin |
title_full | Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin |
title_fullStr | Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin |
title_full_unstemmed | Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin |
title_short | Respiratory Pathways Reconstructed by Multi-Omics Analysis in Melioribacter roseus, Residing in a Deep Thermal Aquifer of the West-Siberian Megabasin |
title_sort | respiratory pathways reconstructed by multi-omics analysis in melioribacter roseus, residing in a deep thermal aquifer of the west-siberian megabasin |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5492636/ https://www.ncbi.nlm.nih.gov/pubmed/28713355 http://dx.doi.org/10.3389/fmicb.2017.01228 |
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