Palmer, Jessica Louise (2019) The degradation of atmospheric pollutants by phyllosphere microbiota. PhD thesis, University of Warwick.

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Abstract

The above-ground parts of plants, termed the phyllosphere, is a largely unexplored microbial habitat that impacts both host plants and global biogeochemical cycles. Previous work established that the phyllosphere is host to an abundance of microbiota, some of which utilise atmospherically derived organic compounds such as phenol and 4-chlorophenol as carbon and energy sources. Many organic compounds in the atmosphere are of anthropogenic origin and considered air pollutants, reducing air quality and increasing human morbidity and mortality rates. This thesis explored the taxonomic and functional diversity of tree phyllospheres, with a focus on the impacts of air pollution on the phyllosphere and the capabilities of tree phyllosphere microbiota to degrade two common atmospheric pollutants: para-nitrophenol (PNP) and carbon monoxide (CO).

The phyllosphere of two common British trees, hawthorn (Crataegus monogyna) and holly (Ilex aquifolium), was characterised by high-throughput sequencing of the 16S rRNA and ITS amplicons to determine how tree species, location and season affect microbial community composition. All variables had a significant impact on the microbial community and preliminary investigations into the impacts of air quality on the phyllosphere population indicated that hawthorn trees sampled by the roadside were enriched with some species from genera known to degrade aromatic compounds such as Variovorax and Aureobasidium.

Culture-dependent and culture-independent techniques were used to determine the potential of hawthorn and holly tree microbiota to degrade PNP and CO. PNP was fully degraded by phyllosphere samples from all tree species, sampling locations and sampling events (n=40). Phyllosphere communities from holly consistently degraded PNP faster than those from hawthorn whereas there was no significant difference in PNP degradation rates between phyllosphere communities of hawthorn trees sampled from woodland or roadside. Four PNP-degrading isolates were identified as species of Pseudomonas, Cabelleronia and Rhodococcus. MiSeq sequencing of 16S rRNA genes and metagenomics of PNP enrichment culture samples provided evidence for xxiii additional candidate PNP-degrading bacteria, indicating that species of Actinomycetospora and Rhizobiales are also likely capable of PNP degradation.

CO was degraded beyond the detectable limit (<50 ppm) by all phyllosphere samples from one timepoint (n=12). As with PNP, CO was degraded significantly faster by holly phyllosphere samples than hawthorn. One CO-degrading strain was isolated and identified as a Mesorhizobium species. Analysis of 16S rRNA genes in samples from CO enrichment cultures with or without an additional carbon source identified a variety of further candidate CO-oxidisers from the Proteobacteria and Actinobacteria phyla. Construction of coxL gene clone libraries from CO enrichment culture samples indicated that a diverse range of coxL genes were present, with nine clades of genes taxonomically similar to species of Rhizobiales, Burkholderiales and Actinomycetales.

Using fine particulate matter (PM2.5) concentration models, hawthorn trees were sampled from areas of high and low pollutant exposure. 16S rRNA and ITS amplicon sequencing data indicated that the composition of both the bacterial and fungal communities were significantly impacted by predicted pollutant exposure. However, the diversity of the bacterial community was not significantly impacted by air quality whereas fungal diversity was impacted. A number of operational taxonomic units (OTUs) from genera known to contain pollutant-degrading species were enriched in the urban phyllosphere, although PNP and CO enrichment culture experiments indicated that phyllosphere samples from more polluted areas degraded these compounds more slowly than less polluted phyllosphere samples.

Overall, this work indicates that PNP and CO degradation are previously unknown potential functions of the phyllosphere of trees. In addition, it is shown that air quality significantly impacts the community composition of bacteria and fungi in the phyllosphere, which in turn is likely to impact the function of phyllosphere microbiota in urban and rural landscapes.

Item Type:	Thesis or Dissertation (PhD)
Subjects:	Q Science > QH Natural history Q Science > QK Botany Q Science > QR Microbiology
Library of Congress Subject Headings (LCSH):	Plants -- Microbiology, Trees -- Microbiology, Air -- Pollution, Pollution prevention, Pollutants -- Biodegradation
Official Date:	September 2019
Dates:	Date Event September 2019 UNSPECIFIED
Institution:	University of Warwick
Theses Department:	School of Life Sciences
Thesis Type:	PhD
Publication Status:	Unpublished
Supervisor(s)/Advisor:	Schäfer, Hendrik ; Bending, G. D. (Gary D.)
Format of File:	pdf
Extent:	xxiii, 311 leaves : colour illustrations
Language:	eng

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