Microbiome and ecology of a hot spring-microbialite system on the Trans-Himalayan Plateau

Abstract

Little is known about life in the boron-rich hot springs of trans-Himalayas. Here, we explore the geomicrobiology of a 4438-m-high spring which emanates ~70 °C-water from a boratic microbialite called Shivlinga. Due to low atmospheric pressure, the vent-water is close to boiling point so can entropically destabilize biomacromolecular systems. Starting from the vent, Shivlinga's geomicrobiology was revealed along the thermal gradients of an outflow-channel and a progressivelydrying mineral matrix that has no running water; ecosystem constraints were then considered in relation to those of entropically comparable environments. the spring-water chemistry and sinter mineralogy were dominated by borates, sodium, thiosulfate, sulfate, sulfite, sulfide, bicarbonate, and other macromolecule-stabilizing (kosmotropic) substances. Microbial diversity was high along both of the hydrothermal gradients. Bacteria, eukarya and Archaea constituted >98%, ~1% and <1% of Shivlinga's microbiome, respectively. Temperature constrained the biodiversity at ~50 °C and ~60 °C, but not below 46 °C. Along each thermal gradient, in the vent-to-apron trajectory, communities were dominated by Aquificae/Deinococcus-Thermus, then Chlorobi/Chloroflexi/Cyanobacteria, and finally Bacteroidetes/Proteobacteria/Firmicutes. interestingly, sites of >45 °C were inhabited by phylogenetic relatives of taxa for which laboratory growth is not known at >45 °C. Shivlinga's geomicrobiology highlights the possibility that the system's kosmotrope-dominated chemistry mitigates against the biomacromolecule-disordering effects of its thermal water. The microbial ecologies of habitats that are hydrothermal, or hypersaline, have been well-characterized, and can give insights into the origins of early life on Earth 1-3. Both chaotrope-rich hypersaline brines and high-temperature freshwater systems can entropically disorder the macromolecules of cellular systems, and are in this way analogous as microbial habitats 4-7. Indeed, highly-chaotropic and hydrothermal habitats are comparable at various scales of biology: the biomacromolecule, cellular system, and functional ecosystem 8,9. Chaotropic, hypersaline habitats include the MgCl 2-constrained ecosystems located at the interfaces of some of the stratified deep-sea hypersaline brines and their overlying seawater. Biophysical, culture-based, and metagenomic studies of the steep haloclines found at these interfaces have revealed that macromolecule-disordering (chaotropic) activities of MgCl 2 not only determine microbial community composition, but also limit Earth's functional biosphere 5,7,10 in such locations, as in situ microbial communities stop functioning at 2.2-2.4 M MgCl 2

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