Cultivation-independent Investigation of Archaeal Diversity in Geothermal Habitats
Open Access DepositedThe aim of my dissertation is to examine archaeal diversity and ecology using metagenomics in various geothermal habitats including the little-understood Hawaiian steam vents and lava caves, the hot spring and geyser sinters of El Tatio, Northern Chile, which is the third largest geyser field in the world after Yellowstone, USA, and Dolina Geizerov, Russia, and previously unsampled hot spring sites in Turkey including the Kula-Salihli UNESCO GeoPark to expand our knowledge about their evolutionary history, metabolic potential, and function in global nutrient cycles. Since the discovery of archaea about 45 years ago, the number of archaeal lineages having cultured representatives remains low. I used a culture-independent computational approach that enables the reconstruction of archaeal genomes (metagenome-assembled genomes, MAGs) directly from environmental samples. I was interested in the MAGs belonging to the novel members of Thaumarchaeota and its sister lineage Aigarchaeota. Ammonia-oxidizing Thaumarchaeota are among the most abundant archaea on Earth. They play major roles in the cycling of nitrogen in the oceans and soil, and significantly contribute to the emission of the greenhouse gas nitrous oxide, indicating strong links with climate change. Genomic exploration of the potential cellular and physiological properties of the novel Thaumarchaeota could offer further insights into their lifestyle, diversification and adaptation mechanisms in the understudied ecosystems and provide implications for climate change mitigation efforts. Evolutionarily close relationship of Aigarchaeota with Thaumarchaeota renders them a key archaeal group to investigate the origin of ammonia oxidation capability in Thaumarchaeota. Analyses of the MAGs could also shed new light into the timing of the divergence of these two groups and their adaptation to the rise of oxygen in the early Earth's atmosphere around 2.3 billion years ago. In this context, novel family (Calditenuaceae), genus (Pelearchaeum), and species (Pelearchaeum maunauluense and Calditenuis fumarioli) of Aigarchaeota were proposed based on MAGs derived from lava rock samples from fumaroles in Mauna Ulu volcanic area in Hawai‘i, and these novel taxa names were validated under the SeqCode Registry, a new code of prokaryotic nomenclature for uncultured microbes. Moreover, the gene content analysis of proviral regions identified in the MAGs of the novel members of Aigarchaeota showed that several auxiliary metabolic genes encoded by proviruses may confer a fitness advantage on their hosts by increasing their metabolic potential and make them better adapted to new environmental conditions. Furthermore, I identified ten distinct casposons in the Thaumarchaeota MAGs obtained from biofilms of Hawaiian fumaroles along with other types of integrated mobile genetic elements (IMGEs) such as transposons and conjugative and cryptic elements. Similar to the proviruses of Aigarchaeota, the unique gene clusters carried by IMGEs found in Thaumarchaeota MAGs harbor a diverse range of functional potential, which suggests that IMGEs could play significant roles in the fitness and survival of their thaumarchaeal hosts. These observations corroborate the hypothesis that IMGEs are major agents of molecular innovation and environmental adaptation of cellular organisms (in some cases, symbionts of their hosts) rather than being ‘junk DNA’ or ‘genomic parasites’. Lastly, the survey of microbial diversity in geothermal environments in Turkey, which employed high-throughput 16S rRNA gene sequencing and metagenome assembly and binning, revealed large proportions of unclassified microorganisms and high taxonomic novelty, which is usually regarded as a marker for endemicity. Intriguingly, the characterization of CRISPR-Cas systems of Nanoarchaeota genomes recovered from hot spring sediments in UNESCO GeoPark unraveled the presence of subtype V-F CRISPR-Cas system encoding a unique effector protein distantly related to Cas14a, which is a recently discovered miniature CRISPR protein with a potential to be utilized for high-fidelity detection of DNA single-nucleotide polymorphisms. This finding highlights the diversity of CRISPR systems hidden in uncultivated organisms. Ongoing genomic exploration of microbial lineages underrepresented in public databases will likely give rise to continued development of CRISPR-based biotechnological applications.
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