Terrestrial hot spring environments: prokaryotic adaptation to extreme conditions and biological contributions to geologic records

Abstract

Terrestrial hot spring environments are of ecological and astrobiological interest owing to their broad spectrum of physicochemistries, including extreme temperatures and pHs. Nevertheless, ecological insights into the distribution of hot spring microbial communities across wide-ranging temperatures and pHs, including their adaptation to extreme physicochemical conditions, are scarce. Therefore, this thesis explored the distribution of microbial communities associated with sinters and sediments across various hot spring physicochemistries in the Taupo Volcanic Zone, New Zealand. Results showed positive correlations between microbial community alpha diversity and decreasing temperatures and increasing pHs. Community composition was significantly influenced by temperature, pH, and water chemistry. Furthermore, a positive correlation between copy numbers of prokaryotic 16S and eukaryotic 18S rRNA genes were identified with decreasing temperatures, while no trend was observed with pH. Molecular and scanning electron microscopy approaches were used to unveil the intimate association between digitate sinter and microbial communities but showed no relationship between community composition and digitate sinter morphological variation. Moreover, metagenomics was used to determine the adaptation mechanisms underpinning the distribution of the bacterial genus, Acidithiobacillus, across wide-ranging hot spring physicochemistries. Results showed that hot spring-associated Acidithiobacillus possess unique adaptation strategies, such as having high GC and proline-encoding contents, and streamlined genomes, potentially allowing them to live up to 40°C higher than previously known type strains (ranging from 17.5- 92.9°C). These Acidithiobacillus also possessed various pH homeostasis proteins, such as amino acid decarboxylases and Na+/H+ antiporters, that may facilitate them to inhabit hot spring pHs ranging from 1.0-7.5. To further explore the extent of cosmopolitanism among hot spring microorganisms, this thesis examined the distribution of abundant hot spring taxa via analysis of 16S rRNA gene amplicon sequence variants. Results identified cosmopolitan variants from diverse phyla across wide-ranging temperatures and pHs, suggesting this is a common feature of hot spring microorganisms. This thesis not only provides ecological insights into the distribution and adaptation of hot spring microorganisms across broad spectrum of temperatures and pHs but also advances our understanding of microbial roles as biosignatures in the geological records of hot springs, which aids astrobiological interpretations of early life on Earth and putative extraterrestrial life.