Biogeography of photoheterotrophic microbes in coastal waters of Australia
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Marine microbes control the flux of energy and chemicals in the ocean and therefore mediate ocean productivity and biogeochemistry, which ultimately sustains marine life and controls global climate. A numerically and functionally important group of marine microbes, for which there is currently a significant gap in knowledge regarding their ecology and biogeography, are the photoheterotrophic bacteria. These microbes, including both Aerobic Anoxygenic Phototrophic Bacteria (AAnPB) and proteorhodopsin based phototrophic bacteria and Archaea (PRBA) comprise up to 70% of microbial communities within surface waters of the ocean. Capable of gaining energy from light-induced proton translocation and from the oxidation of organic material, these often highly abundant bacteria have been proposed to significantly influence marine biogeochemistry and trophodynamics. However, the environmental (i.e. physicochemical, seasonal, oceanographic) factors influencing the abundance and diversity of these organisms are currently poorly defined, particularly within the often highly productive waters of the Southern Hemisphere. The aim of this thesis was to examine changes in photoheterotrophic community abundance and composition in coastal waters of Australia and identify the key environmental influences on the ecology of these microbes. Samples collected from a combination of oceanographic research voyages and time-series sampling regimes were analysed using both amplicon sequencing approaches and quantitative PCR targeting 𝑝𝑢𝑓M and proteorhodopsin genes to characterise AAnPB and PRBA populations respectively. High temporal resolution analysis of photohetetrophic bacterial population dynamics in the coastal waters of Australia indicated seasonality in the abundance and diversity of these groups. Along the eastern coast of Australia, AAnPB abundance was highly variable, with 𝑝𝑢𝑓M gene copies ranging from 1.1 x 10² to 1.4 x 10⁵ mL⁻¹, and positively correlated with day length and solar radiation. 𝑝𝑢𝑓M gene amplicon sequencing revealed that the majority of sequences were closely related to those obtained previously in other environments, suggesting that key AAnPB groups are widely distributed across similar environments globally. Temperature was a major structuring factor for AAnPB assemblages across large spatial scales, correlating positively with richness and Gammaproteobacteria (phylogroup K) abundance, but negatively with Roseobacter-clade (phylogroup E) abundance, with temperatures between 16-18 °C identified as a potential transition zone between these groups. Coastal PRBA assemblages were also dynamic in both space and time, with diversity correlated to indicators of waterbody oligotrophy including positively to temperature, Secchi depth and Prochlorococcus cell abundance and negatively to phosphate concentration. Shifts in taxonomic composition were best explained by temperature and day length. Seasonality in taxonomic structure was accompanied by temporal variability in proteorhodopsin spectral tuning. Finally, we provide evidence for spatial transitions in the abundance and diversity of key photoheterotrophic bacterial groups between different oceanographic provinces within northern Australian waters, indicating that shifts in physical and biotic characteristics can lead to sharp changes in the importance of these important marine microbial assemblages across water masses. Total bacterial abundance was higher in ATS waters, which was reflected by higher AAnPB abundance in this region, whereas the major proteorhodopsin containing clade, SAR11, displayed the opposite trend, with higher abundances in the Coral Sea. Among the AAnPB, the Gammaproteobacterial phylogroup K dominated the community in both regions, with relatively stable composition of AAnPB across regions. Conversely, the PRBA community displayed clear differences between the two regions, with the Arafura Timor Sea (ATS) dominated by SAR11-like and Betaproteobacterial sequences, while the Coral Sea was dominated by Archaea group IIb and members of SAR11 clade A and B. In conclusion, this thesis has demonstrated how dynamic these populations are and that each of these two groups should not be treated as single population, but one that is comprised of many interacting and potentially competing units, that are each governed by different environmental factors and thereby fill discrete niches.
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