Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C
ABSTRACT Gammaproteobacterial methanotrophic bacteria (gMOB) are dominant methanotrophs in the water column of oxygen-stratified boreal and subarctic lakes and ponds. (Meta)genomic data suggest that, besides methane (CH4), gMOB potentially use dissolved organic matter (DOM) and reduced sulfur compou...
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American Society for Microbiology
2025-07-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03133-24 |
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| author | Antti Juhani Rissanen Rahul Mangayil Alexander T. Tveit Susanna T. Maanoja Ramita Khanongnuch |
| author_facet | Antti Juhani Rissanen Rahul Mangayil Alexander T. Tveit Susanna T. Maanoja Ramita Khanongnuch |
| author_sort | Antti Juhani Rissanen |
| collection | DOAJ |
| description | ABSTRACT Gammaproteobacterial methanotrophic bacteria (gMOB) are dominant methanotrophs in the water column of oxygen-stratified boreal and subarctic lakes and ponds. (Meta)genomic data suggest that, besides methane (CH4), gMOB potentially use dissolved organic matter (DOM) and reduced sulfur compounds (e.g., sulfide) as electron sources. To study the DOM and sulfide metabolism of lake gMOB, we subjected a psychrophilic lake water strain, Methylobacter sp. S3L5C, first to different sulfide levels (Na2S, 0–5 mM) to test the toxicity, and subsequently, to freshwater DOM (60 mg L−1) either alone or with sulfide (0.05 mM) at 1 and 20% CH4 levels. The growth, CH4 and O2 consumption, CO2 production, and mRNA expression patterns of S3L5C were analyzed. Sulfide concentrations of 0–0.5 mM had no effect, while 1 and 5 mM concentrations inhibited the strain’s growth. At 20% CH4, DOM addition enhanced CH4 consumption, CO2 production, and growth of S3L5C, while the addition of sulfide+DOM led to further increases in these variables. The addition of sulfide+DOM enhanced CH4 consumption even at 1% CH4. The effect of DOM on the S3L5C’s metabolism was accompanied by enhanced expression of the cyc2 gene, which has been suggested to mediate the extracellular electron transfer from DOM. Furthermore, the addition of sulfide+DOM enhanced the expression of the sqr and soxB genes encoding dissimilatory sulfide and thiosulfate oxidation, respectively. Together with previous metagenomic data, these results suggest that the usage of DOM and reduced sulfur compounds as electron sources is a trait that enhances methanotrophy among gMOB of boreal and subarctic lakes and ponds.IMPORTANCEGammaproteobacterial methanotrophic bacteria (gMOB) are crucial mitigators of methane emissions of many ecosystems, like boreal and subarctic lakes and ponds. Metagenomic data suggest that besides using methane, gMOB have genetic potential to use dissolved organic matter (DOM) and sulfide, typically present in lakes and ponds, as electron donors. To test the effect of DOM and sulfide on the methane metabolism of gMOB of oxygen-stratified boreal lakes, we subjected our recently isolated lake gMOB strain, Methylobacter sp. S3L5C, to additions of freshwater DOM and sulfide. We show that DOM and sulfide enhance methane consumption and growth of S3L5C. Furthermore, the expression of genes mediating the electron transfer from DOM and sulfide is enhanced. Our results suggest that the usage of DOM and reduced sulfur compounds as electron sources is a trait that enhances methanotrophy among gMOB and adds significantly to the growing body of literature highlighting the enormous metabolic versatility of gMOB. |
| format | Article |
| id | doaj-art-5bcadc7deb4744faaf52267e906adae4 |
| institution | DOAJ |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | American Society for Microbiology |
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| spelling | doaj-art-5bcadc7deb4744faaf52267e906adae42025-08-20T03:16:00ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-07-0113710.1128/spectrum.03133-24Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5CAntti Juhani Rissanen0Rahul Mangayil1Alexander T. Tveit2Susanna T. Maanoja3Ramita Khanongnuch4Faculty of Engineering and Natural Sciences, Tampere University, Tampere, Pirkanmaa, FinlandDepartment of Bioproducts and Biosystems, School of Chemical Engineering, Aalto University, Espoo, FinlandDepartment of Arctic and Marine Biology, UiT, The Arctic University of Norway, Tromsø, Troms, NorwayFaculty of Engineering and Natural Sciences, Tampere University, Tampere, Pirkanmaa, FinlandFaculty of Engineering and Natural Sciences, Tampere University, Tampere, Pirkanmaa, FinlandABSTRACT Gammaproteobacterial methanotrophic bacteria (gMOB) are dominant methanotrophs in the water column of oxygen-stratified boreal and subarctic lakes and ponds. (Meta)genomic data suggest that, besides methane (CH4), gMOB potentially use dissolved organic matter (DOM) and reduced sulfur compounds (e.g., sulfide) as electron sources. To study the DOM and sulfide metabolism of lake gMOB, we subjected a psychrophilic lake water strain, Methylobacter sp. S3L5C, first to different sulfide levels (Na2S, 0–5 mM) to test the toxicity, and subsequently, to freshwater DOM (60 mg L−1) either alone or with sulfide (0.05 mM) at 1 and 20% CH4 levels. The growth, CH4 and O2 consumption, CO2 production, and mRNA expression patterns of S3L5C were analyzed. Sulfide concentrations of 0–0.5 mM had no effect, while 1 and 5 mM concentrations inhibited the strain’s growth. At 20% CH4, DOM addition enhanced CH4 consumption, CO2 production, and growth of S3L5C, while the addition of sulfide+DOM led to further increases in these variables. The addition of sulfide+DOM enhanced CH4 consumption even at 1% CH4. The effect of DOM on the S3L5C’s metabolism was accompanied by enhanced expression of the cyc2 gene, which has been suggested to mediate the extracellular electron transfer from DOM. Furthermore, the addition of sulfide+DOM enhanced the expression of the sqr and soxB genes encoding dissimilatory sulfide and thiosulfate oxidation, respectively. Together with previous metagenomic data, these results suggest that the usage of DOM and reduced sulfur compounds as electron sources is a trait that enhances methanotrophy among gMOB of boreal and subarctic lakes and ponds.IMPORTANCEGammaproteobacterial methanotrophic bacteria (gMOB) are crucial mitigators of methane emissions of many ecosystems, like boreal and subarctic lakes and ponds. Metagenomic data suggest that besides using methane, gMOB have genetic potential to use dissolved organic matter (DOM) and sulfide, typically present in lakes and ponds, as electron donors. To test the effect of DOM and sulfide on the methane metabolism of gMOB of oxygen-stratified boreal lakes, we subjected our recently isolated lake gMOB strain, Methylobacter sp. S3L5C, to additions of freshwater DOM and sulfide. We show that DOM and sulfide enhance methane consumption and growth of S3L5C. Furthermore, the expression of genes mediating the electron transfer from DOM and sulfide is enhanced. Our results suggest that the usage of DOM and reduced sulfur compounds as electron sources is a trait that enhances methanotrophy among gMOB and adds significantly to the growing body of literature highlighting the enormous metabolic versatility of gMOB.https://journals.asm.org/doi/10.1128/spectrum.03133-24methanotrophmethane oxidationMethylobacterlakepondgreenhouse gas |
| spellingShingle | Antti Juhani Rissanen Rahul Mangayil Alexander T. Tveit Susanna T. Maanoja Ramita Khanongnuch Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C Microbiology Spectrum methanotroph methane oxidation Methylobacter lake pond greenhouse gas |
| title | Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C |
| title_full | Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C |
| title_fullStr | Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C |
| title_full_unstemmed | Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C |
| title_short | Dissolved organic matter and sulfide enhance the CH4 consumption of a psychrophilic lake methanotroph, Methylobacter sp. S3L5C |
| title_sort | dissolved organic matter and sulfide enhance the ch4 consumption of a psychrophilic lake methanotroph methylobacter sp s3l5c |
| topic | methanotroph methane oxidation Methylobacter lake pond greenhouse gas |
| url | https://journals.asm.org/doi/10.1128/spectrum.03133-24 |
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