Diversity and distribution of the lanthanome in aerobic methane-oxidising bacteria

Background

Lanthanides (Ln) play important and often regulatory roles in the metabolism of methylotrophs, including methanotrophs, particularly through their involvement in methanol oxidation. However, the diversity, distribution, and ecological relevance of Ln-associated proteins (the lanthanome) in aerobic methane-oxidising bacteria (MOB) remain underexplored. This study investigates the lanthanome using genome, plasmid, and proteome data, alongside metatranscriptome data from methane-rich lake sediments.

Results

We surveyed 179 genomes spanning Proteobacterial, Verrucomicrobial, and Actinobacterial MOBs to examine the distribution of Ln-dependent methanol dehydrogenases (MDHs) and Ln transport proteins. Distinct lineage-specific patterns were observed: XoxF5 was the most widespread MDH variant in Proteobacteria, while XoxF2 was restricted to Verrucomicrobia. Transporter systems also showed distinct patterns, with LanM restricted to Alphaproteobacteria, LanPepSY and LanA confined to Gammaproteobacteria, and LutH-like receptors broadly distributed across all lineages. Homologues of these genes were also detected on plasmids, indicating potential for horizontal gene transfer. In Lake Washington sediment metatranscriptomes, lanthanome transcripts were detected, with Proteobacteria as dominant contributors. Notably, a large fraction of xoxF transcripts were affiliated with non-MOB Methylophilaceae, consistent with known cooperative interactions with MOB. Using Methylosinus trichosporium OB3b as a model, we assessed methane oxidation and proteomic responses to soluble CeCl3 and a mixed-lanthanide ore. Lag phases were prolonged in the presence of lanthanides, particularly with ore, but methane oxidation rates converged across treatments after acclimation. Proteomic analysis revealed extensive condition-specific responses, with 724 proteins differentially expressed in Ore treatment compared to 60 under CeCl3. XoxF3 and XoxF5 were upregulated while MxaF and its accessory proteins were downregulated, consistent with the “lanthanide switch”. Notably, LanM was not expressed despite being encoded, whereas LutH-like receptor was downregulated under both treatments, likely reflecting regulatory control to prevent excess metal uptake. Additional upregulation of a TonB-dependent receptor and ABC transporter suggests a potential lanthanophore-mediated uptake strategy.

Conclusion

This study highlights the diversity and ecological activity of Ln-binding and transport systems in MOBs, their plasmid localisation and potential mobility, and their distinct regulation under different Ln sources. The strong proteomic response to complex ore underscores the physiological flexibility of MOBs in coping with natural lanthanide forms. These findings provide a framework for ecological studies and candidate targets for biotechnological applications in methane bioconversion and sustainable lanthanide recovery from complex materials.

Exploring the Role of Lanthanides in Methane-Eating Bacteria

What is it about?

The study investigated the diversity, distribution, and ecological relevance of lanthanide-associated proteins (the lanthanome) in aerobic methane-oxidising bacteria (MOB) using a combination of genomic, plasmid, proteomic, and metatranscriptomic data. A survey of 179 MOB genomes across Proteobacterial, Verrucomicrobial, and Actinobacterial lineages was conducted to examine the distribution of lanthanide-dependent methanol dehydrogenases (MDHs) and transport proteins. Lineage-specific patterns were observed, with XoxF5 being widespread in Proteobacteria and XoxF2 restricted to Verrucomicrobia, while transporter systems showed clade-specific distributions. In environmental metatranscriptomes from Lake Washington sediments, lanthanome transcripts were detected predominantly from Proteobacteria, with notable contributions from non-MOB Methylophilaceae. Laboratory experiments with Methylosinus trichosporium OB3b indicated extended lag phases in the presence of lanthanides, particularly with mixed-lanthanide ore, although methane oxidation rates eventually converged across treatments. Proteomic analysis revealed condition-specific responses, with XoxF enzymes upregulated and MxaF downregulated, highlighting a ""lanthanide switch"" mechanism. The study underscored the physiological flexibility of MOBs in adapting to natural lanthanide forms and the potential for horizontal gene transfer of lanthanide-associated genes.

Why is it important?

This study is important as it sheds light on the ecological and metabolic roles of lanthanides in aerobic methane-oxidising bacteria (MOB), contributing to our understanding of microbial methane metabolism and its potential applications. By exploring the diversity and distribution of lanthanide-associated proteins (the lanthanome) in various MOB lineages, the research highlights the significance of lanthanides in methanol oxidation and methane bioconversion processes. The findings open avenues for biotechnological applications aimed at methane mitigation and sustainable lanthanide recovery, providing insights into microbial adaptation and resilience in lanthanide-rich environments.

Key Takeaways:

1. Diverse Lanthanome Distribution: The study reveals that lanthanoenzymes such as XoxF are broadly distributed across MOB phyla, with xoxF5 being the most prevalent in Proteobacteria. This highlights the evolutionary significance and widespread role of lanthanides in methanol dehydrogenase activity among MOBs.

2. Clade-specific Lanthanide Transporters: The research identifies distinct clade-specific patterns in lanthanide transporter distribution, with LanM restricted to Alphaproteobacteria and LanPepSY and LanA confined to Gammaproteobacteria. This suggests varied molecular strategies for lanthanide uptake across different MOB lineages.

3. Proteomic Responses to Lanthanides: The study observes condition-specific proteomic responses in MOBs exposed to soluble CeCl₃ and mixed-lanthanide ore, indicating physiological flexibility in natural lanthanide forms. The differential expression of proteins such as XoxF3 and XoxF5 underlines the adaptive mechanisms of MOBs to varying lanthanide sources.