Tree phyllospheres are a habitat for diverse populations of CO-oxidising bacteria

Abstract

AbstractBackgroundCarbon monoxide (CO) is a naturally occurring and ubiquitous trace gas in the atmosphere. As a product of combustion processes, it can reach concentrations in the mg/m3 range in urban areas, contributing to air pollution. Aerobic CO-degrading microorganisms have been identified previously and are thought to remove ~370 Tg of CO in soils and oceans per year. Based on the presence of genes encoding subunits of the enzyme carbon monoxide dehydrogenase in metagenomes, a large fraction of soil bacteria may have the potential for CO degradation. The activity and diversity of CO-degrading microorganisms in above ground habitats such as the phyllosphere has not been addressed, however, and their potential role in global CO cycling remains unknown.ResultsMonitoring of CO-degradation in leaf washes of two common British trees, Ilex aquifolium and Crataegus monogyna, demonstrated CO uptake in all samples investigated. Leaf washes of I. aquifolium had significantly higher CO oxidation rates than those of C. monogyna. A diverse range of bacterial taxa were identified as candidate CO-oxidising taxa based on high-throughput sequencing and multivariate statistical analysis of 16S rRNA amplicon data, as well as functional diversity analysis based on coxL, the gene encoding the large subunit of CO-dehydrogenase. Candidate CO-oxidising taxa included a range of Rhizobiales and Burkholderiales, of which the Burkholderiales OTUs were abundant colonisers of the phyllosphere at the time of sampling, as indicated by 16S rRNA gene sequencing. In addition, an estimated 12.4% of leaf OTUs in samples of this study contained coxL homologues, based on their predicted genomes. We also mined data of publicly available phyllosphere metagenomes for genes encoding subunits of CO-dehydrogenase which indicated that, on average, 25% of phyllosphere bacteria contained CO-dehydrogenase gene homologues. A CO-oxidising Phyllobacteriaceae strain was isolated from phyllosphere samples which contains genes encoding both CODH as well as a RuBisCO.ConclusionsThe phyllosphere, a vast microbial habitat, supports diverse and potentially abundant CO-oxidising bacteria. These findings identify tree phyllosphere bacteria as a potential sink for atmospheric CO and highlight the need for a more detailed assessment of phyllosphere microbial communities in the global cycle of CO.