<italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments
ABSTRACT Methane-oxidizing microorganisms perform an important role in reducing emissions of the greenhouse gas methane to the atmosphere. To date, known bacterial methanotrophs belong to the Proteobacteria, Verrucomicrobia, and NC10 phyla. Within the Proteobacteria phylum, they can be divided into...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-06-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00631-18 |
| _version_ | 1818683641414287360 |
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| author | Mohammad Ghashghavi Svetlana E. Belova Paul L. E. Bodelier Svetlana N. Dedysh Martine A. R. Kox Daan R. Speth Peter Frenzel Mike S. M. Jetten Sebastian Lücker Claudia Lüke |
| author_facet | Mohammad Ghashghavi Svetlana E. Belova Paul L. E. Bodelier Svetlana N. Dedysh Martine A. R. Kox Daan R. Speth Peter Frenzel Mike S. M. Jetten Sebastian Lücker Claudia Lüke |
| author_sort | Mohammad Ghashghavi |
| collection | DOAJ |
| description | ABSTRACT Methane-oxidizing microorganisms perform an important role in reducing emissions of the greenhouse gas methane to the atmosphere. To date, known bacterial methanotrophs belong to the Proteobacteria, Verrucomicrobia, and NC10 phyla. Within the Proteobacteria phylum, they can be divided into type Ia, type Ib, and type II methanotrophs. Type Ia and type II are well represented by isolates. Contrastingly, the vast majority of type Ib methanotrophs have not been able to be cultivated so far. Here, we compared the distributions of type Ib lineages in different environments. Whereas the cultivated type Ib methanotrophs (Methylococcus and Methylocaldum) are found in landfill and upland soils, lineages that are not represented by isolates are mostly dominant in freshwater environments, such as paddy fields and lake sediments. Thus, we observed a clear niche differentiation within type Ib methanotrophs. Our subsequent isolation attempts resulted in obtaining a pure culture of a novel type Ib methanotroph, tentatively named “Methylotetracoccus oryzae” C50C1. Strain C50C1 was further characterized to be an obligate methanotroph, containing C16:1ω9c as the major membrane phospholipid fatty acid, which has not been found in other methanotrophs. Genome analysis of strain C50C1 showed the presence of two pmoCAB operon copies and XoxF5-type methanol dehydrogenase in addition to MxaFI. The genome also contained genes involved in nitrogen and sulfur cycling, but it remains to be demonstrated if and how these help this type Ib methanotroph to adapt to fluctuating environmental conditions in freshwater ecosystems. IMPORTANCE Most of the methane produced on our planet gets naturally oxidized by a group of methanotrophic microorganisms before it reaches the atmosphere. These microorganisms are able to oxidize methane, both aerobically and anaerobically, and use it as their sole energy source. Although methanotrophs have been studied for more than a century, there are still many unknown and uncultivated groups prevalent in various ecosystems. This study focused on the diversity and adaptation of aerobic methane-oxidizing bacteria in different environments by comparing their phenotypic and genotypic properties. We used lab-scale microcosms to create a countergradient of oxygen and methane for preenrichment, followed by classical isolation techniques to obtain methane-oxidizing bacteria from a freshwater environment. This resulted in the discovery and isolation of a novel methanotroph with interesting physiological and genomic properties that could possibly make this bacterium able to cope with fluctuating environmental conditions. |
| first_indexed | 2024-12-17T10:37:58Z |
| format | Article |
| id | doaj.art-7e07d142d48c4073b73faa67bcb22088 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-17T10:37:58Z |
| publishDate | 2019-06-01 |
| publisher | American Society for Microbiology |
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| series | mSphere |
| spelling | doaj.art-7e07d142d48c4073b73faa67bcb220882022-12-21T21:52:20ZengAmerican Society for MicrobiologymSphere2379-50422019-06-014310.1128/mSphere.00631-18<italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater EnvironmentsMohammad Ghashghavi0Svetlana E. Belova1Paul L. E. Bodelier2Svetlana N. Dedysh3Martine A. R. Kox4Daan R. Speth5Peter Frenzel6Mike S. M. Jetten7Sebastian Lücker8Claudia Lüke9Department of Microbiology, IWWR, Radboud University, Nijmegen, the NetherlandsResearch Center of Biotechnology of the Russian Academy of Sciences, Winogradski Institute of Microbiology, Moscow, RussiaDepartment of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, the NetherlandsResearch Center of Biotechnology of the Russian Academy of Sciences, Winogradski Institute of Microbiology, Moscow, RussiaDepartment of Microbiology, IWWR, Radboud University, Nijmegen, the NetherlandsDepartment of Microbiology, IWWR, Radboud University, Nijmegen, the NetherlandsMax Planck Institute for Terrestrial Microbiology, Marburg, GermanyDepartment of Microbiology, IWWR, Radboud University, Nijmegen, the NetherlandsDepartment of Microbiology, IWWR, Radboud University, Nijmegen, the NetherlandsDepartment of Microbiology, IWWR, Radboud University, Nijmegen, the NetherlandsABSTRACT Methane-oxidizing microorganisms perform an important role in reducing emissions of the greenhouse gas methane to the atmosphere. To date, known bacterial methanotrophs belong to the Proteobacteria, Verrucomicrobia, and NC10 phyla. Within the Proteobacteria phylum, they can be divided into type Ia, type Ib, and type II methanotrophs. Type Ia and type II are well represented by isolates. Contrastingly, the vast majority of type Ib methanotrophs have not been able to be cultivated so far. Here, we compared the distributions of type Ib lineages in different environments. Whereas the cultivated type Ib methanotrophs (Methylococcus and Methylocaldum) are found in landfill and upland soils, lineages that are not represented by isolates are mostly dominant in freshwater environments, such as paddy fields and lake sediments. Thus, we observed a clear niche differentiation within type Ib methanotrophs. Our subsequent isolation attempts resulted in obtaining a pure culture of a novel type Ib methanotroph, tentatively named “Methylotetracoccus oryzae” C50C1. Strain C50C1 was further characterized to be an obligate methanotroph, containing C16:1ω9c as the major membrane phospholipid fatty acid, which has not been found in other methanotrophs. Genome analysis of strain C50C1 showed the presence of two pmoCAB operon copies and XoxF5-type methanol dehydrogenase in addition to MxaFI. The genome also contained genes involved in nitrogen and sulfur cycling, but it remains to be demonstrated if and how these help this type Ib methanotroph to adapt to fluctuating environmental conditions in freshwater ecosystems. IMPORTANCE Most of the methane produced on our planet gets naturally oxidized by a group of methanotrophic microorganisms before it reaches the atmosphere. These microorganisms are able to oxidize methane, both aerobically and anaerobically, and use it as their sole energy source. Although methanotrophs have been studied for more than a century, there are still many unknown and uncultivated groups prevalent in various ecosystems. This study focused on the diversity and adaptation of aerobic methane-oxidizing bacteria in different environments by comparing their phenotypic and genotypic properties. We used lab-scale microcosms to create a countergradient of oxygen and methane for preenrichment, followed by classical isolation techniques to obtain methane-oxidizing bacteria from a freshwater environment. This resulted in the discovery and isolation of a novel methanotroph with interesting physiological and genomic properties that could possibly make this bacterium able to cope with fluctuating environmental conditions.https://journals.asm.org/doi/10.1128/mSphere.00631-18methaneaerobic methane oxidationcomparative genomicspaddy fieldsoil microbiome |
| spellingShingle | Mohammad Ghashghavi Svetlana E. Belova Paul L. E. Bodelier Svetlana N. Dedysh Martine A. R. Kox Daan R. Speth Peter Frenzel Mike S. M. Jetten Sebastian Lücker Claudia Lüke <italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments mSphere methane aerobic methane oxidation comparative genomics paddy field soil microbiome |
| title | <italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments |
| title_full | <italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments |
| title_fullStr | <italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments |
| title_full_unstemmed | <italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments |
| title_short | <italic toggle="yes">Methylotetracoccus oryzae</italic> Strain C50C1 Is a Novel Type Ib Gammaproteobacterial Methanotroph Adapted to Freshwater Environments |
| title_sort | italic toggle yes methylotetracoccus oryzae italic strain c50c1 is a novel type ib gammaproteobacterial methanotroph adapted to freshwater environments |
| topic | methane aerobic methane oxidation comparative genomics paddy field soil microbiome |
| url | https://journals.asm.org/doi/10.1128/mSphere.00631-18 |
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