Hot in Cold: Microbial Life in the Hottest Springs in Permafrost

Abstract

Chukotka is an arctic region located in the continuous permafrost zone, but thermal springs are abundant there. In this study, for the first time, the microbial communities of the Chukotka hot springs (CHS) biofilms and sediments with temperatures 54-94 °C were investigated and analyzed by NGS sequencing of 16S rRNA gene amplicons. In microbial mats (54-75 °C), phototrophic bacteria of genus <i>Chloroflexus</i> dominated (up to 89% of all prokaryotes), while <i>Aquificae</i> were the most numerous at higher temperatures in Fe-rich sediments and filamentous "streamers" (up to 92%). The electron donors typical for <i>Aquificae</i>, such as H₂S and H₂, are absent or present only in trace amounts, and the prevalence of <i>Aquificae</i> might be connected with their ability to oxidize the ferrous iron present in CHS sediments. <i>Armatimonadetes</i>, <i>Proteobacteria</i>, <i>Deinococcus-Thermus</i>, <i>Dictyoglomi</i>, and <i>Thermotogae,</i> as well as uncultured bacteria (candidate divisions Oct-Spa1-106, GAL15, and OPB56), were numerous, and <i>Cyanobacteria</i> were present in low numbers. Archaea (less than 8% of the total community of each tested spring) belonged to <i>Bathyarchaeota</i>, <i>Aigarchaeota</i>, and <i>Thaumarchaeota</i>. The geographical location and the predominantly autotrophic microbial community, built on mechanisms other than the sulfur cycle-based ones, make CHS a special and unique terrestrial geothermal ecosystem.