Methanol utilizers of the rhizosphere and phyllosphere of a common grass and forb host species

Abstract

Background Managed grasslands are global sources of atmospheric methanol, which is one of the most abundant volatile organic compounds in the atmosphere and promotes oxidative capacity for tropospheric and stratospheric ozone depletion. The phyllosphere is a favoured habitat of plant-colonizing methanol-utilizing bacteria. These bacteria also occur in the rhizosphere, but their relevance for methanol consumption and ecosystem fluxes is unclear. Methanol utilizers of the plant-associated microbiota are key for the mitigation of methanol emission through consumption. However, information about grassland plant microbiota members, their biodiversity and metabolic traits, and thus key actors in the global methanol budget is largely lacking. Results We investigated the methanol utilization and consumption potentials of two common plant species (Festuca arundinacea and Taraxacum officinale) in a temperate grassland. The selected grassland exhibited methanol formation. The detection of 13C derived from 13C-methanol in 16S rRNA of the plant microbiota by stable isotope probing (SIP) revealed distinct methanol utilizer communities in the phyllosphere, roots and rhizosphere but not between plant host species. The phyllosphere was colonized by members of Gamma- and Betaproteobacteria. In the rhizosphere, 13C-labelled Bacteria were affiliated with Deltaproteobacteria, Gemmatimonadates, and Verrucomicrobiae. Less-abundant 13C-labelled Bacteria were affiliated with well-known methylotrophs of Alpha-, Gamma-, and Betaproteobacteria. Additional metagenome analyses of both plants were consistent with the SIP results and revealed Bacteria with methanol dehydrogenases (e.g., MxaF1 and XoxF1-5) of known but also unusual genera (i.e., Methylomirabilis, Methylooceanibacter, Gemmatimonas, Verminephrobacter). 14C-methanol tracing of alive plant material revealed divergent potential methanol consumption rates in both plant species but similarly high rates in the rhizosphere and phyllosphere. Conclusions Our study revealed the rhizosphere as an overlooked hotspot for methanol consumption in temperate grasslands. We further identified unusual new but potentially relevant methanol utilizers besides well-known methylotrophs in the phyllosphere and rhizosphere. We did not observe a plant host-specific methanol utilizer community. Our results suggest that our approach using quantitative SIP and metagenomics may be useful in future field studies to link gross methanol consumption rates with the rhizosphere and phyllosphere microbiome.

Genome‐resolved metagenomics identifies novel active microbes in biogeochemical cycling within methanol‐enriched soil

“…The methanol-enriched wheat rhizosphere soils exclusively contained MAGs identified as Gemmatimonadales, Roseimicrobium and Nitrososphaeraceae. This supports the prior identification of a greater diversity of these specific taxa in the methanolenriched rhizosphere soils relative to the unplanted soils (Macey et al, 2020), with many of the taxa previously identified as enriched in rhizosphere soils (e.g., Chthoniobacter [Sangwan et al, 2004], Nitrososphaeraceae [Prudence et al, 2021], Methylophilaceae [Kanukollu et al, 2022;Macey et al, 2020], and species within the Acidobacteriota and Verrucomicrobiota [Da Rocha et al, 2013;Lanzavecchia et al, 2024]).…”

Metabolic coupling between soil aerobic methanotrophs and denitrifiers in rice paddy fields

“…Nevertheless, we acknowledge that the specific coupling pathways of CH 4 oxidation and denitrification may vary among different strains and within diverse microbial communities. For instance, the results from 13 CH 4 -SIP indicate that Rhizobia , as carriers of denitrification gene nirK , have the potential to utilize C from CH 4 , but with specific metabolic pathways remaining unclear 50 , 51 . Therefore, additional studies, such as isolating these specific taxa in pure culture and utilizing third-generation metagenomic approaches to obtain higher quality MAGs, are warranted to reinforce and consolidate the findings presented in this study.…”