The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation
ABSTRACT Methane is a potent greenhouse gas in the atmosphere, and its concentration has continued to increase in recent decades. Aerobic methanotrophs, bacteria that use methane as the sole carbon source, are an important biological sink for methane, and they are widely distributed in the natural e...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-06-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.00247-22 |
| _version_ | 1818249229048479744 |
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| author | Julie Scanlan Richard Guillonneau Mark R. Cunningham Sahanara Najmin Michaela A. Mausz Andrew Murphy Leanne L. Murray Limei Zhang Deepak Kumaresan Yin Chen |
| author_facet | Julie Scanlan Richard Guillonneau Mark R. Cunningham Sahanara Najmin Michaela A. Mausz Andrew Murphy Leanne L. Murray Limei Zhang Deepak Kumaresan Yin Chen |
| author_sort | Julie Scanlan |
| collection | DOAJ |
| description | ABSTRACT Methane is a potent greenhouse gas in the atmosphere, and its concentration has continued to increase in recent decades. Aerobic methanotrophs, bacteria that use methane as the sole carbon source, are an important biological sink for methane, and they are widely distributed in the natural environment. However, relatively little is known on how methanotroph activity is regulated by nutrients, particularly phosphorus (P). P is the principal nutrient constraining plant and microbial productivity in many ecosystems, ranging from agricultural land to the open ocean. Using a model methanotrophic bacterium, Methylosinus trichosporium OB3b, we demonstrate here that this bacterium can produce P-free glycolipids to replace membrane phospholipids in response to P limitation. The formation of the glycolipid monoglucuronic acid diacylglycerol requires plcP-agt genes since the plcP-agt mutant is unable to produce this glycolipid. This plcP-agt-mediated lipid remodeling pathway appears to be important for M. trichosporium OB3b to cope with P stress, and the mutant grew significantly slower under P limitation. Interestingly, comparative genomics analysis shows that the ability to perform lipid remodeling appears to be a conserved trait in proteobacterial methanotrophs; indeed, plcP is found in all proteobacterial methanotroph genomes, and plcP transcripts from methanotrophs are readily detectable in metatranscriptomics data sets. Together, our study provides new insights into the adaptation to P limitation in this ecologically important group of bacteria. IMPORTANCE Methane is a potent greenhouse gas in the atmosphere, and its concentration has continued to increase steadily in recent decades. In the natural environment, bacteria known as methanotrophs help mitigate methane emissions at no cost to human beings. However, relatively little is known regarding how methane oxidation activity in methanotrophs is regulated by soil nutrients, particularly phosphorus. Here, we show that methanotrophs can modify their membrane in response to phosphorus limitation and that the ability to change membrane lipids is important for methanotroph activity. Genome and metatranscriptome analyses suggest that such an adaptation strategy appears to be strictly conserved in all proteobacterial methanotrophs and is used by these bacteria in the natural environment. Together, our study provides a plausible molecular mechanism for better understanding the role of phosphorus on methane oxidation in the natural environment. |
| first_indexed | 2024-12-12T15:33:10Z |
| format | Article |
| id | doaj.art-40e51c77d8814624bd170dec07c2b864 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-12T15:33:10Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-40e51c77d8814624bd170dec07c2b8642022-12-22T00:20:04ZengAmerican Society for MicrobiologymBio2150-75112022-06-0113310.1128/mbio.00247-22The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate LimitationJulie Scanlan0Richard Guillonneau1Mark R. Cunningham2Sahanara Najmin3Michaela A. Mausz4Andrew Murphy5Leanne L. Murray6Limei Zhang7Deepak Kumaresan8Yin Chen9School of Life Sciences, University of Warwick, Coventry, UKSchool of Life Sciences, University of Warwick, Coventry, UKSchool of Biological Sciences, Queen’s University Belfast, Belfast, UKSchool of Life Sciences, University of Warwick, Coventry, UKSchool of Life Sciences, University of Warwick, Coventry, UKSchool of Life Sciences, University of Warwick, Coventry, UKSchool of Biological Sciences, Queen’s University Belfast, Belfast, UKSchool of Life Sciences, University of Warwick, Coventry, UKSchool of Biological Sciences, Queen’s University Belfast, Belfast, UKSchool of Life Sciences, University of Warwick, Coventry, UKABSTRACT Methane is a potent greenhouse gas in the atmosphere, and its concentration has continued to increase in recent decades. Aerobic methanotrophs, bacteria that use methane as the sole carbon source, are an important biological sink for methane, and they are widely distributed in the natural environment. However, relatively little is known on how methanotroph activity is regulated by nutrients, particularly phosphorus (P). P is the principal nutrient constraining plant and microbial productivity in many ecosystems, ranging from agricultural land to the open ocean. Using a model methanotrophic bacterium, Methylosinus trichosporium OB3b, we demonstrate here that this bacterium can produce P-free glycolipids to replace membrane phospholipids in response to P limitation. The formation of the glycolipid monoglucuronic acid diacylglycerol requires plcP-agt genes since the plcP-agt mutant is unable to produce this glycolipid. This plcP-agt-mediated lipid remodeling pathway appears to be important for M. trichosporium OB3b to cope with P stress, and the mutant grew significantly slower under P limitation. Interestingly, comparative genomics analysis shows that the ability to perform lipid remodeling appears to be a conserved trait in proteobacterial methanotrophs; indeed, plcP is found in all proteobacterial methanotroph genomes, and plcP transcripts from methanotrophs are readily detectable in metatranscriptomics data sets. Together, our study provides new insights into the adaptation to P limitation in this ecologically important group of bacteria. IMPORTANCE Methane is a potent greenhouse gas in the atmosphere, and its concentration has continued to increase steadily in recent decades. In the natural environment, bacteria known as methanotrophs help mitigate methane emissions at no cost to human beings. However, relatively little is known regarding how methane oxidation activity in methanotrophs is regulated by soil nutrients, particularly phosphorus. Here, we show that methanotrophs can modify their membrane in response to phosphorus limitation and that the ability to change membrane lipids is important for methanotroph activity. Genome and metatranscriptome analyses suggest that such an adaptation strategy appears to be strictly conserved in all proteobacterial methanotrophs and is used by these bacteria in the natural environment. Together, our study provides a plausible molecular mechanism for better understanding the role of phosphorus on methane oxidation in the natural environment.https://journals.asm.org/doi/10.1128/mbio.00247-22Methylosinuslipid remodelingmethanotroph |
| spellingShingle | Julie Scanlan Richard Guillonneau Mark R. Cunningham Sahanara Najmin Michaela A. Mausz Andrew Murphy Leanne L. Murray Limei Zhang Deepak Kumaresan Yin Chen The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation mBio Methylosinus lipid remodeling methanotroph |
| title | The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation |
| title_full | The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation |
| title_fullStr | The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation |
| title_full_unstemmed | The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation |
| title_short | The Proteobacterial Methanotroph Methylosinus trichosporium OB3b Remodels Membrane Lipids in Response to Phosphate Limitation |
| title_sort | proteobacterial methanotroph methylosinus trichosporium ob3b remodels membrane lipids in response to phosphate limitation |
| topic | Methylosinus lipid remodeling methanotroph |
| url | https://journals.asm.org/doi/10.1128/mbio.00247-22 |
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