Dimitry Y. Sorokin , Alexander Y. Merkel , William Gebbe , Marina G. Kalyuzhnaya
{"title":"Thiohalorhabdus methylotropha sp. nov., an extremely halophilic autotrophic methylotiotroph from hypersaline lakes","authors":"Dimitry Y. Sorokin , Alexander Y. Merkel , William Gebbe , Marina G. Kalyuzhnaya","doi":"10.1016/j.syapm.2025.126602","DOIUrl":null,"url":null,"abstract":"<div><div>So far, there have been no reports of trimethylamine (TMA)-utilizing extremely halophilic microorganisms in hypersaline habitats. Our aerobic enrichments at 4 M total Na<sup>+</sup> with 5 mM TMA inoculated with surface sediments from hypersaline soda (at pH 9.5) or chloride-sulfate (at pH 7) lakes in southwestern Siberia were successful only for the latter. The initial enrichment included both bacteria and haloarchaea but only the bacterial component was able to grow as a pure culture with TMA. Strain Cl-TMA forms a new-species lineage within the genus <em>Thiohalorhabdus</em> which includes extremely halophilic and obligate lithoautotrophic sulfur-oxidizing gammaproteobacteria. Cl-TMA can grow methyloautotrophically utilizing TMA, dimethylamine (DMA) and methanol (MeOH) as the electron donors or chemolithoautotrophically with thiosulfate. Mixotrophic growth was also observed with the three methyl compounds and thiosulfate. Carbon is assimilated autotrophically via the Calvin-Benson-Basham pathway. Unlike the type species of <em>Thiohalorhabdus</em>, <em>T. denitrificans</em>, Cl-TMA was incapable of anaerobic growth via denitrification. The isolate belongs to extreme halophiles growing between 2.5 and 5 M NaCl with an optimum at 3–3.5 M. Genome analysis identified two gene clusters coding for PQQ-dependent methanol dehydrogenases (MxaFI and XoxF), four homologues of the formaldehyde activating enzymes (Faes), a TMA/DMA oxidation locus, and two cluster of genes encoding an <em>N</em>-methylglutamate dehydrogenase pathway (NMGP) for methylamine oxidation. The first steps of C<sub>1</sub>-subtrate conversions are followed by the tetrahydrofolate (THF)-linked and tetrahydromethanopterin (H4MPT)-linked formaldehyde oxidation pathways and two formate dehydrogenases. All of those signatures of methylotrophy were absent in <em>T. denitrificans</em>. In contrast, genes for two key sulfur oxidation enzymes, thiosulfate dehydrogenase TsdAB and sulfide dehydrogenase FccAB, that are present in the type species are missing in Cl-TMA. Thiosulfate is oxidized to sulfate by a combination of an incomplete Sox cycle and an sHdr system. Strain Cl-TMA<sup>T</sup> (JCM 35977 = UQM 41915) is proposed to be classified as <em>Thiohalorhabdus methylotrophus</em> sp. nov.</div></div>","PeriodicalId":22124,"journal":{"name":"Systematic and applied microbiology","volume":"48 3","pages":"Article 126602"},"PeriodicalIF":3.3000,"publicationDate":"2025-03-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Systematic and applied microbiology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0723202025000244","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
So far, there have been no reports of trimethylamine (TMA)-utilizing extremely halophilic microorganisms in hypersaline habitats. Our aerobic enrichments at 4 M total Na+ with 5 mM TMA inoculated with surface sediments from hypersaline soda (at pH 9.5) or chloride-sulfate (at pH 7) lakes in southwestern Siberia were successful only for the latter. The initial enrichment included both bacteria and haloarchaea but only the bacterial component was able to grow as a pure culture with TMA. Strain Cl-TMA forms a new-species lineage within the genus Thiohalorhabdus which includes extremely halophilic and obligate lithoautotrophic sulfur-oxidizing gammaproteobacteria. Cl-TMA can grow methyloautotrophically utilizing TMA, dimethylamine (DMA) and methanol (MeOH) as the electron donors or chemolithoautotrophically with thiosulfate. Mixotrophic growth was also observed with the three methyl compounds and thiosulfate. Carbon is assimilated autotrophically via the Calvin-Benson-Basham pathway. Unlike the type species of Thiohalorhabdus, T. denitrificans, Cl-TMA was incapable of anaerobic growth via denitrification. The isolate belongs to extreme halophiles growing between 2.5 and 5 M NaCl with an optimum at 3–3.5 M. Genome analysis identified two gene clusters coding for PQQ-dependent methanol dehydrogenases (MxaFI and XoxF), four homologues of the formaldehyde activating enzymes (Faes), a TMA/DMA oxidation locus, and two cluster of genes encoding an N-methylglutamate dehydrogenase pathway (NMGP) for methylamine oxidation. The first steps of C1-subtrate conversions are followed by the tetrahydrofolate (THF)-linked and tetrahydromethanopterin (H4MPT)-linked formaldehyde oxidation pathways and two formate dehydrogenases. All of those signatures of methylotrophy were absent in T. denitrificans. In contrast, genes for two key sulfur oxidation enzymes, thiosulfate dehydrogenase TsdAB and sulfide dehydrogenase FccAB, that are present in the type species are missing in Cl-TMA. Thiosulfate is oxidized to sulfate by a combination of an incomplete Sox cycle and an sHdr system. Strain Cl-TMAT (JCM 35977 = UQM 41915) is proposed to be classified as Thiohalorhabdus methylotrophus sp. nov.
期刊介绍:
Systematic and Applied Microbiology deals with various aspects of microbial diversity and systematics of prokaryotes. It focuses on Bacteria and Archaea; eukaryotic microorganisms will only be considered in rare cases. The journal perceives a broad understanding of microbial diversity and encourages the submission of manuscripts from the following branches of microbiology: