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• W114101242 abstract "Methane is a potent greenhouse gas, approximately 30 times more effective in trapping heat than carbon dioxide, and contributes significantly to global warming. In nature, methane can be produced and consumed by microbes. One of the most important methane sinks is anaerobic oxidation of methane (AOM), which is responsible for substantial consumption of methane from anoxic environments by coupling its oxidation to various electron acceptors. This thesis aims to understand the microorganisms associated with AOM coupled to nitrate reduction, a process that is of increasing environmental relevance as water bodies become eutrophied through endemic use of fertilisers for agriculture. The first report of a consortium capable of AOM coupled to denitrification was reported in 2006, comprised of an anaerobic methanotrophic (ANME) archaea belonging to the family ANME-2d, now known as Candidatus Methanoperedens nitroreducens, and a bacterial member Candidatus Methlomirabilis oxyfera. However, long-term incubations demonstrate that the M. nitroreducens can be absent from the process and that M. oxyfera is capable of performing AOM alone by coupling to nitrite reduction. The disappearance of M. nitroreducens brought into question its role in the initial consortium. Here, microbial community profiling of nitrate-driven AOM reactors showed that M. nitroreducens dominated the community. In Chapter Two, a novel method that modified the conventional fluorescence in situ hybridisation (FISH) by removing the fixation-step and separated cells of interest using fluorescence activated cell sorting (FACS), was developed with the goal of sequencing single-cells of M. nitroreducens. This fixation-free method was believed to eliminate the crosslinking of protein and nucleic acid by fixatives, thus increasing the nucleic acid yield for sequencing. As a proof of concept, the fixation-free FISH-FACS method was successfully applied to populations of monoderm and diderm cells. Using an optimised approach, single cells and populations of M. nitroreducens were separated away from other community members for genome sequencing. These results are presented as a published book chapter. To further elucidate the role of M. nitroreducens in nitrate-driven AOM, detailed analysis of metagenomic, single-cell genomics and metatranscriptomics data was undertaken in Chapter Three. Results showed that M. nitroreducens was capable of independent AOM through reverse methanogenesis using nitrate as the terminal electron acceptor. Comparative analyses revealed that the genes for nitrate reduction appear to be laterally transferred from a bacterial donor, suggesting selection for this novel process within M. nitroreducens. Nitrite produced by M. nitroreducens was reduced to dinitrogen gas through a syntrophic relationship with an anaerobic ammonium-oxidizing bacterium. These results are presented as a published manuscript. In Chapter Four, eight reactor communities fed with different combinations of methane, nitrate, nitrite and ammonium were characterised using 16S ribosomal RNA gene amplicon sequencing and validated using FISH. Results showed that core populations (Methanoperedeneceae, Kuenenia and Methylomirabilis) were stable across reactors but present at different abundances suggestive of competitive and cooperative interactions between populations. Deep amplicon sequencing revealed a diverse community including three previously unrecognized bacterial populations; Ignavibacteriales (belonging to the phylum Chlorobi), Phycisphaerales (belonging to the phylum Planctomycetes) and Anaerolineae (belonging to the phylum Chloroflexi). Ignavibacteriales abundance correlated with high nitrite consumption rates suggesting its role in nitrite reduction. Phycisphaerales had an inverse relationship with Kuenenia and Ignavibacteriales suggesting that there may be competitive interactions and that Phycisphaerales may also have a similar role in nitrite reduction. The ubiquity of Anaerolineae in most reactors indicated that it may be a generalist. These results are presented as a draft manuscript. Genomic evidence indicates that M. nitroreducens is not only able to reduce nitrate to nitrite but also nitrite to ammonium, in a process called dissimilatory nitrate reduction to ammonium (DNRA). DNRA is a major part of the nitrogen cycle and catalysed by the cytochrome c nitrite reductases (nrfA). M. nitroreducens has three copies of nrfA, making this the first report of nrfA in an archaeon. Chapter Five applied meta-omic approaches, coupled to stable isotope labelling tests, to characterise a reactor community performing AOM coupled to DNRA. Stable isotope labelling tests showed accumulation of 15N-labelled ammonium in batch reactor with high carbon to nitrogen ratio. Metagenomics showed similar members of the community as described in Chapter Four and were consistently dominated by M. nitroreducens. Using a differential coverage binning approach, 20 near-complete population genomes were extracted. Gene-centric analysis indicated that a number of the populations had the genes for nitrate reduction (napA and narG) and nitrite ammonification (nrfA), but only two known methanotrophs (M. nitroreducens and Candidatus Methylomirabilis oxyfera) harboured key genes for methane oxidation (mcrA and pmoA), respectively. However, most of M. nitroreducens’ expressed genes were in the top 5% of absolute transcript counts, showing that M. nitroreducens is the most active population in the reactor. The M. nitroreducens’ mcr complex was differentially expressed but its nrfAs were not significantly expressed in the AOM-DNRA batch reactor and several other members of the community also demonstrated low levels of nrfA expression. These results may suggest that 1) DNRA may have already been occurring in the nitrate-driven AOM batch reactor, 2) other bacterial populations together with M. nitroreducens may collectively be carrying out DNRA or 3) the gene expression of nrfA may not correlate to the cytochrome c nitrite reductase protein abundance. Future metaproteomics will be required to confirm this finding. The findings presented in this thesis have provided new insight into the structure of microbial communities in nitrate-driven AOM and the highlighted potential interplay between specific populations." @default.
• W114101242 created "2016-06-24" @default.
• W114101242 creator A5064918522 @default.
• W114101242 date "2015-01-29" @default.
• W114101242 modified "2023-09-24" @default.
• W114101242 title "Molecular characterisation of microbial communities involved in nitrate-driven anaerobic oxidation of methane" @default.
• W114101242 doi "https://doi.org/10.14264/uql.2015.220" @default.
• W114101242 hasPublicationYear "2015" @default.
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