Microbial biogeography of 1,000 geothermal springs: spatial, temporal, and allopatric dynamics of extremophiles in the Taupō Volcanic Zone, Aotearoa-New Zealand
Permanent link to Research Commons versionhttps://hdl.handle.net/10289/15754
Geothermal springs are model ecosystems to investigate microbial biogeography as they represent discrete, relatively homogeneous habitats, are distributed across multiple geographical scales, and span broad geochemical gradients. This thesis reports the largest consolidated study of geothermal ecosystems to determine causal factors that influence both spatial and temporal biogeographical patterns of extremophiles. Bacterial and archaeal community composition, 46 physicochemical parameters, and metadata from 925 geothermal spring water columns across the Taupō Volcanic Zone (TVZ), Aotearoa-New Zealand were measured. Standardised methodologies were employed to define microbial diversity via 16S rRNA gene amplicon sequencing, and associated physicochemistry, ensuring confidence in sample comparison. Over an 8,000 km² spatial scale, multivariate statistical analyses determined diversity was primarily influenced by pH at temperatures <70 °C; with temperature only having a significant effect at >70 °C. Further, community dissimilarity increased with increasing geographic distance across the region, highlighting niche selection driving assembly at a local scale. This research also describes the first comprehensive temporal study of geothermal microbial communities in Aotearoa-New Zealand. One hundred and fifteen water column samples from 31 geothermal features were taken over a 34-month period to ascertain microbial community stability, community response to both natural and anthropogenic disturbances in the local environment, and temporal variation in spring diversity across the pH range found in the TVZ. Results indicated temperature and associated groundwater physicochemistry were the most likely parameters to vary stochastically in these geothermal features, with community abundances rather than composition more readily affected by a changing environment. However, variation in pH (pH ±1) had a more significant effect on community structure than temperature (±20 °C), with alpha diversity failing to be an adequate measure of temporal microbial disparity in geothermal features outside of circumneutral conditions. While a substantial physicochemical disturbance was required to shift community structures at the phylum level, geothermal ecosystems were resilient at this broad taxonomic rank and returned to a pre-disturbed state if environmental conditions re-established. The discovery that genus 𝑉𝑒𝑛𝑒𝑛𝑖𝑣𝑖𝑏𝑟𝑖𝑜 (phylum Aquificota) exhibited the greatest average abundance (11.2 %) and distribution (74.2 %) of all taxa across 925 geothermal ecosystems in the TVZ, and an apparent absence of this taxon in global geothermal systems, led to the hypothesis that allopatric speciation enabled the evolution of an endemic bacterial genus to Aotearoa-New Zealand. Maximal read abundance of 𝑉𝑒𝑛𝑒𝑛𝑖𝑣𝑖𝑏𝑟𝑖𝑜 occurred in geothermal features with pH 4-6, 50-70 °C, and low oxidation-reduction potentials, highlighting a specific environmental niche that could enhance habitat isolation. Genomic analysis of the only characterised species for the genus, 𝑉𝑒𝑛𝑒𝑛𝑖𝑣𝑖𝑏𝑟𝑖𝑜 𝑠𝑡𝑎𝑔𝑛𝑖𝑠𝑝𝑢𝑚𝑎𝑛𝑡𝑖𝑠 CP.B2ᵀ, confirmed a chemolithoautotrophic metabolism dependent on hydrogen oxidation. While similarity between 𝑉𝑒𝑛𝑒𝑛𝑖𝑣𝑖𝑏𝑟𝑖𝑜 populations illustrated dispersal was not limited across the TVZ, extensive amplicon, metagenomic, and phylogenomic analyses of local and global microbial communities from DNA sequence databases indicated 𝑉𝑒𝑛𝑒𝑛𝑖𝑣𝑖𝑏𝑟𝑖𝑜 is geographically restricted to the Aotearoa-New Zealand archipelago. It was concluded that combined geographical and physicochemical constraints prevent this taxon from distributing on a broader scale, resulting in the establishment of an endemic bacterial genus. Collectively, the findings from this thesis provide an insight into ecological behaviour in geothermal springs, highlighting the diverse controls between different taxa within the same habitat-type, and expand understanding of microbial biogeography in extreme ecosystems.
The University of Waikato
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