Mesophilic inmates of a geothermal vent–head as providers of critical ecosystem services

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Abstract

Geothermal vent–heads exclusively support the proliferation of (hyper)thermophilic microorganisms. However, diverse mesophiles are stochastically thrust into these ecosystems by local geodynamic forces, and their population–level responses to the unfamiliar stressor hold critical implications for life′s intrinsic resilience to biophysical adversities. Here, we report a time–course exploration of the boiling vent–water of a Trans–Himalayan geothermal spring to determine the population dynamics, in situ functionalities, and potential ecological roles of mesophilic incomers in the context of indigenous (hyper)thermophiles. The temporally–consistent (hyper)thermophilic core–community, predominated in turn by a few Aquificia and Thermoproteota, was delineated as m etagenome– a ssembled g enomes. Mesophiles/moderate–thermophiles were identified as MAG s and/or pure–cultures, and whether temporally–consistent/inconsistent, had far lower prevalence. Overall, in situ transcriptional activity and prevalence had significant positive correlation; but many species exhibited high activity despite low prevalence and vice versa, implicating the decoupling of global metabolism from growth/proliferation. Bulked metatranscriptomic signatures identified the (hyper)thermophiles as primary producers of the ecosystem. Populations of mesophiles and moderate–thermophiles were apparently active, but not growing, in situ , with some being engaged in environment detoxification, and production of nutrients, metabolites and protective–biomolecules wanting in the (hyper)thermophiles. The findings engender an unprecedented portrayal of geothermal–vents as multi–community ecosystems where unfamiliar immigrants provide critical metabolic services.

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