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

Jess L Palmer,Sally Hilton,Emma Picot,Gary D Bending,Hendrik Schäfer

doi:10.1111/1462-2920.15770

Abstract

Carbon monoxide (CO) is both a ubiquitous atmospheric trace gas and an air pollutant. While aerobic CO-degrading microorganisms in soils and oceans are estimated to remove ~370 Tg of CO per year, the presence of CO-degrading microorganisms in above-ground habitats, such as the phyllosphere, and their potential role in CO cycling remains unknown. CO-degradation by leaf washes of two common British trees, Ilex aquifolium and Crataegus monogyna, demonstrated CO uptake in all samples investigated. Based on the analyses of taxonomic and functional genes, diverse communities of candidate CO-oxidizing taxa were identified, including members of Rhizobiales and Burkholderiales which were abundant in the phyllosphere at the time of sampling. Based on predicted genomes of phyllosphere community members, an estimated 21% of phyllosphere bacteria contained CoxL, the large subunit of CO-dehydrogenase. In support of this, data mining of publicly available phyllosphere metagenomes for genes encoding CO-dehydrogenase subunits demonstrated that, on average, 25% of phyllosphere bacteria contained CO-dehydrogenase gene homologues. A CO-oxidizing Phyllobacteriaceae strain was also isolated from phyllosphere samples which contains genes encoding both CO-dehydrogenase as well as a ribulose-1,5-bisphosphate carboxylase-oxygenase. These results suggest that the phyllosphere supports diverse and potentially abundant CO-oxidizing bacteria, which are a potential sink for atmospheric CO.

Highlights

The phyllosphere, defined as the above ground parts of plants, is a vast microbial habitat covering an estimated surface area of around 1 billion km2 (Woodward and Lomas, 2004; Vorholt, 2012)
Leaf wash filters were used as an inoculum for Carbon monoxide (CO) enrichment cultures containing 800 ppm CO plus an additional carbon source of yeast extract to encourage the growth of heterotrophic CO oxidizers
Incubation of leaf wash samples from all three sample types, woodland hawthorn (HtW), roadside hawthorn (HtR) and woodland holly (HlW) in mineral medium amended with yeast extract resulted in the degradation of 800 ppm CO (Fig. 1)

Summary

Introduction

The phyllosphere, defined as the above ground parts of plants, is a vast microbial habitat covering an estimated surface area of around 1 billion km (Woodward and Lomas, 2004; Vorholt, 2012). It is colonized by diverse microorganisms including fungi, archaea, protists, viruses and bacteria, of which bacteria are the most abundant group, with an estimated 106–107 bacterial cells per cm of leaf (Lindow and Brandl, 2003). Activities of phyllosphere bacteria affect atmospheric chemistry and the fate of atmospheric pollutants and may contribute to critical ecosystem services of the phyllosphere in mitigation of air pollution, a major global public health problem causing around 5.5 million premature deaths worldwide (Lelieveld et al, 2015)

Results

Discussion

Conclusion