Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems
Abstract Lakes and ponds are considered as a major natural source of CH4 emissions, particularly during the ice-free period in boreal ecosystems. Aerobic methane-oxidizing bacteria (MOB), which utilize CH4 using oxygen as an electron acceptor, are one of the dominant microorganisms in the CH4-rich w...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Oxford University Press
2022-09-01
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| Series: | ISME Communications |
| Online Access: | https://doi.org/10.1038/s43705-022-00172-x |
| _version_ | 1797227112580513792 |
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| author | Ramita Khanongnuch Rahul Mangayil Mette Marianne Svenning Antti Juhani Rissanen |
| author_facet | Ramita Khanongnuch Rahul Mangayil Mette Marianne Svenning Antti Juhani Rissanen |
| author_sort | Ramita Khanongnuch |
| collection | DOAJ |
| description | Abstract Lakes and ponds are considered as a major natural source of CH4 emissions, particularly during the ice-free period in boreal ecosystems. Aerobic methane-oxidizing bacteria (MOB), which utilize CH4 using oxygen as an electron acceptor, are one of the dominant microorganisms in the CH4-rich water columns. Metagenome-assembled genomes (MAGs) have revealed the genetic potential of MOB from boreal aquatic ecosystems for various microaerobic/anaerobic metabolic functions. However, experimental proof of these functions, i.e., organic acid production via fermentation, by lake MOB is lacking. In addition, psychrophilic (i.e., cold-loving) MOB and their CH4-oxidizing process have rarely been investigated. In this study, we isolated, provided a taxonomic description, and analyzed the genome of Methylobacter sp. S3L5C, a psychrophilic MOB, from a boreal lake in Finland. Based on phylogenomic comparisons to MAGs, Methylobacter sp. S3L5C represented a ubiquitous cluster of Methylobacter spp. in boreal aquatic ecosystems. At optimal temperatures (3–12 °C) and pH (6.8–8.3), the specific growth rates (µ) and CH4 utilization rate were in the range of 0.018–0.022 h−1 and 0.66–1.52 mmol l−1 d−1, respectively. In batch cultivation, the isolate could produce organic acids, and the concentrations were elevated after replenishing CH4 and air into the headspace. Up to 4.1 mM acetate, 0.02 mM malate, and 0.07 mM propionate were observed at the end of the test under optimal operational conditions. The results herein highlight the key role of Methylobacter spp. in regulating CH4 emissions and their potential to provide CH4-derived organic carbon compounds to surrounding heterotrophic microorganisms in cold ecosystems. |
| first_indexed | 2024-04-24T14:35:37Z |
| format | Article |
| id | doaj.art-a3994ffca45c4268809841cf067d0382 |
| institution | Directory Open Access Journal |
| issn | 2730-6151 |
| language | English |
| last_indexed | 2024-04-24T14:35:37Z |
| publishDate | 2022-09-01 |
| publisher | Oxford University Press |
| record_format | Article |
| series | ISME Communications |
| spelling | doaj.art-a3994ffca45c4268809841cf067d03822024-04-03T00:58:56ZengOxford University PressISME Communications2730-61512022-09-012111010.1038/s43705-022-00172-xCharacterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystemsRamita Khanongnuch0Rahul Mangayil1Mette Marianne Svenning2Antti Juhani Rissanen3Faculty of Engineering and Natural Sciences, Tampere UniversityFaculty of Engineering and Natural Sciences, Tampere UniversityDepartment of Arctic and Marine Biology, UiT, The Arctic University of NorwayFaculty of Engineering and Natural Sciences, Tampere UniversityAbstract Lakes and ponds are considered as a major natural source of CH4 emissions, particularly during the ice-free period in boreal ecosystems. Aerobic methane-oxidizing bacteria (MOB), which utilize CH4 using oxygen as an electron acceptor, are one of the dominant microorganisms in the CH4-rich water columns. Metagenome-assembled genomes (MAGs) have revealed the genetic potential of MOB from boreal aquatic ecosystems for various microaerobic/anaerobic metabolic functions. However, experimental proof of these functions, i.e., organic acid production via fermentation, by lake MOB is lacking. In addition, psychrophilic (i.e., cold-loving) MOB and their CH4-oxidizing process have rarely been investigated. In this study, we isolated, provided a taxonomic description, and analyzed the genome of Methylobacter sp. S3L5C, a psychrophilic MOB, from a boreal lake in Finland. Based on phylogenomic comparisons to MAGs, Methylobacter sp. S3L5C represented a ubiquitous cluster of Methylobacter spp. in boreal aquatic ecosystems. At optimal temperatures (3–12 °C) and pH (6.8–8.3), the specific growth rates (µ) and CH4 utilization rate were in the range of 0.018–0.022 h−1 and 0.66–1.52 mmol l−1 d−1, respectively. In batch cultivation, the isolate could produce organic acids, and the concentrations were elevated after replenishing CH4 and air into the headspace. Up to 4.1 mM acetate, 0.02 mM malate, and 0.07 mM propionate were observed at the end of the test under optimal operational conditions. The results herein highlight the key role of Methylobacter spp. in regulating CH4 emissions and their potential to provide CH4-derived organic carbon compounds to surrounding heterotrophic microorganisms in cold ecosystems.https://doi.org/10.1038/s43705-022-00172-x |
| spellingShingle | Ramita Khanongnuch Rahul Mangayil Mette Marianne Svenning Antti Juhani Rissanen Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems ISME Communications |
| title | Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems |
| title_full | Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems |
| title_fullStr | Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems |
| title_full_unstemmed | Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems |
| title_short | Characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous Methylobacter spp. cluster in boreal lake ecosystems |
| title_sort | characterization and genome analysis of a psychrophilic methanotroph representing a ubiquitous methylobacter spp cluster in boreal lake ecosystems |
| url | https://doi.org/10.1038/s43705-022-00172-x |
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