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Lanthanide-dependent methanol dehydrogenase XoxF confers a competitive advantage for occupancy of Medicago sativa nodules by Sinorhizobium meliloti.

ABSTRACT: The recent discovery of the lanthanide(Ln)-dependent methanol dehydrogenase (MDH) XoxF has expanded the spectrum of bacteria recognized for methylotrophic metabolism. Many bacteria, including rhizobia, have long escaped being categorized as methylotrophs because they exclusively produce XoxF-type Ln-dependent MDH and entirely lack the long-studied calcium-dependent MDH MxaFI. We report that the XoxF-type Ln-dependent MDH encoded by the smb20173 gene is the sole MDH that supports methylotrophic growth of Sinorhizobium meliloti. The Ln that consistently supported growth of S. meliloti in minimal media with methanol included lanthanum, cerium, praseodymium, and neodymium. Based on genome, whole-transcriptome, and mutant phenotype analyses, we propose a metabolic model for Ln-dependent methylotrophy in S. meliloti wherein oxidation of one-carbon compounds such as methanol generates the reducing power needed to assimilate carbon via the Calvin-Benson-Bassham cycle. By investigating how these newfound insights about Ln reshape our understanding of the methylotrophic capabilities of rhizobia, we explored how methanol produced by plants has the potential to create a nutritional niche in the rhizosphere. Using a Medicago sativa (alfalfa) nodule occupation assay, we found that the xoxF mutant strain was outcompeted by the wild-type strain only when Ln were available, suggesting that Ln-dependent methylotrophy is a potential nutritional mediator of the rhizobia-legume symbiosis.

ORGANISM(S): Sinorhizobium meliloti

PROVIDER: GSE306118 | GEO | 2026/02/07

REPOSITORIES: GEO

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Project description:The increasing demand for non-food competitive carbon sources such as methanol for biotechnology has brought methanol-utilizing bacteria, so-called methylotrophs, to focus. The product spectrum of natural methylotrophs and their genetic accessibility is limited and as an alternative approach, the introduction of methylotrophic metabolism into a biotechnologically well-established organism, such as Escherichia coli, represents a promising concept. By performing long-term evolution over 600 days, we obtained an E. coli strain that is able to grow on methanol as its sole carbon source at rates comparable to natural methylotrophic organisms. We confirmed that the strain forms its entire biomass from methanol. Furthermore, we sequenced the genome of the evolved strain and compared it to the genome of its ancestor. Intriguingly, we found several hundreds of mutations targeting genes of various functions, such as catalysis and regulation. Like the comparison of the genome before and after evolution, the investigation of the proteome would be of high interest. Proteomics would reveal the consequences of the regulatory mutations found in the genome and provide an overall picture of the adaptations by the cell enabling it to grow on methanol. The increasing demand for non-food competitive carbon sources such as methanol for biotechnology has brought methanol-utilizing bacteria, so-called methylotrophs, to focus. The product spectrum of natural methylotrophs and their genetic accessibility is limited and as an alternative approach, the introduction of methylotrophic metabolism into a biotechnologically well-established organism, such as Escherichia coli, represents a promising concept. By performing long-term evolution over 600 days, we obtained an E. coli strain that is able to grow on methanol as its sole carbon source at rates comparable to natural methylotrophic organisms. We confirmed that the strain forms its entire biomass from methanol. Furthermore, we sequenced the genome of the evolved strain and compared it to the genome of its ancestor. Intriguingly, we found several hundreds of mutations targeting genes of various functions, such as catalysis and regulation. Like the comparison of the genome before and after evolution, the investigation of the proteome would be of high interest. Proteomics would reveal the consequences of the regulatory mutations found in the genome and provide an overall picture of the adaptations by the cell enabling it to grow on methanol.

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Lanthanide-dependent methanol dehydrogenase XoxF confers a competitive advantage for occupancy of Medicago sativa nodules by Sinorhizobium meliloti.

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