Abstract
Urban green areas are highly valued by citizens for their contribution to the quality of life in cities. Plants play an important role in mitigating airborne pollutants and are assisted in this role by the metabolic capacities of the millions of microbial cells that colonize leaf surfaces (phyllosphere). Many factors influence phyllosphere microbial community composition and function, but to what extent does airborne pollution in cities impact the composition of microbial communities and their functional degradation genes? Here we describe the characterization of the phyllospheric bacterial communities of Carpinus betulus L. trees (hornbeam) across three locations: the city center of Warsaw (Poland), a forest in a UNESCO World Heritage Site (Białowieża), and a forest in one of the world’s oldest operational oil fields (Bóbrka). C. betulus contained higher particulate matter (PM) concentrations, with higher concentrations of palladium and radon in the PM, on leaves in Warsaw than in the forests. Volatile organic compound (VOC) analyses of sampled air revealed higher concentrations of butanone methyl propanal, butylbenzene, and cyclohexane in Bóbrka than Warsaw and Białowieża, while in Warsaw, xylene and toluene were higher. Shotgun microbiome sequencing uncovered a dominance of Gammaproteobacteria (71%), mainly Pseudomonas spp., Actinobacteria, Alpha- and Betaproteobacteria, and Firmicutes. Community composition and function differed significantly between the forests and Warsaw city center. Statistically more hydrocarbon degradation genes were found in Białowieża compared to Warsaw and Bóbrka, and in vitro tests of diesel degradation and plant growth promotion traits of culturable representatives revealed that Białowieża held the highest number of bacteria with plant beneficial properties and degradation genes. This study provides the first detailed insights into the microbiome of C. betulus and sets the stage for developing to a more integrated understanding of phyllosphere microbiota in cities, and their relationships with human health.
Highlights
MATERIALS AND METHODSTrees play an important role in scavenging and degrading airborne pollutants, and the combined action of plants and phyllospheric microorganisms for plant bioremediation is known as phylloremediation (Weyens et al, 2015; Wei et al, 2017)
The aims of this work were to perform, for the first time: (i) a phylogenetic characterization of bacterial communities hosted by C. betulus leaves; (ii) an assessment of spatial variability of bacterial phyllosphere communities associated with C. betulus trees located in areas of Poland with different types and levels of pollution (Warsaw city center, Bóbrka oil field, and the Białowieza primeval forest); (iii) an evaluation of air pollution impact on the abundance of linear and aromatic hydrocarbon degradation genes; (iv) a quantitative assessment of the potential of phyllosphere isolates to tolerate and metabolize diesel range organics; and (v) an assessment of plant growth promotion traits of isolated phyllospheric bacteria
For the degradation genes benA, bphA1, dbfA2, npah, and alkane monooxygenase B gene (alkB) (Figure 7A), the highest relative number of aromatic compound– degrading gene hits was found in Białowieza, and in Warsaw, samples Wa22 and Wa24 from the vehicle intersection, compared to the other samples. quantitative polymerase chain reaction (qPCR) analyses of the alkane monooxygenase B (AlkB) gene confirm these findings and show a higher AlkB log copy number in Białowieza compared to Bóbrka and Warsaw (Figure 7B). qPCR results were less conclusive for phenol hydroxylase because of the relatively high site-to-site variation (Figure 7B)
Summary
Trees play an important role in scavenging and degrading airborne pollutants, and the combined action of plants and phyllospheric microorganisms for plant bioremediation is known as phylloremediation (Weyens et al, 2015; Wei et al, 2017). There is evidence of higher uptake rates of airborne phenol by leaves inoculated with hydrocarbonoclastic bacteria compared to surface-sterilized leaves (Sandhu et al, 2007), setting the stage for strategic utilizing of phyllosphere microbiota to combat air pollution. It is estimated that aboveground microbial density reaches 106–107 cells/cm of photosynthetically active leaves, remarkable given the hostile phyllosphere environment (Vorholt, 2012) where microorganisms are exposed to large daily and seasonal fluctuations of temperature and humidity, are exposed to air pollutants, have limited access to nutrients, and are exposed to harmful ultraviolet radiation. Far from being static guests, these microorganisms constantly interact with their host plant in symbiotic relationships
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