Eight Metagenome-assembled Genomes Provide Evidence for Microbial Adaptation in 20,000 to 1,000,000-year-old Siberian Permafrost


Katie Sipes, Abraham Almatari, Alexander Eddie, Daniel Williams, Elena Spirina, Elizaveta Rivkina, Renxing Liang, Tullis Onstott, Tatiana A Vishnivetskaya, Karen G Lloydmicrobes


Permafrost microbes may be metabolically active in microscopic layers of liquid brines, even in ancient soil. Metagenomics can help discern whether permafrost microbes show adaptations to this environment. Thirty-three metagenome-assembled genomes (MAGs) were obtained from six depths (3.5 m to 20 m) of freshly-cored permafrost from the Siberia Kolyma-Indigirka Lowland region. These soils have been continuously frozen for ∼20,000 to 1,000,000 years. Eight of these MAGs were ≥80% complete with <10% contamination and were taxonomically identified as Aminicenantes , Atribacteria , Chloroflexi , and Actinobacteria within bacteria and Thermoprofundales within archaea. MAGs from these taxa have previously been obtained from non-permafrost environments and have been suggested to show adaptations to long-term energy-starvation, but they have never been explored in ancient permafrost. The permafrost MAGs had higher proportions of clusters of orthologous genes (COGs) from ‘Energy production and conversion’ and ‘Carbohydrate transport and metabolism’ than their non-permafrost counterparts. They also contained genes for trehalose synthesis, thymine metabolism, mevalonate biosynthesis and cellulose degradation that were less prevalent in non-permafrost genomes. Many of these genes are involved in membrane stabilization and osmotic stress responses, consistent with adaptation to the anoxic, high ionic strength, cold environments of permafrost brine films. Our results suggest that this ancient permafrost contains DNA in high enough quality to assemble MAGs from microorganisms with adaptations to subsist long-term freezing in this extreme environment. Importance Permafrost around the world is thawing rapidly. Many scientists from a variety of disciplines have shown the importance of understanding what will happen to our ecosystem, commerce, and climate when permafrost thaws. The fate of permafrost microorganisms is connected to these predicted rapid environmental changes. Studying ancient permafrost with culture independent techniques can give a glimpse into how these microorganisms function in these extreme low temperature and energy conditions. This will aid understanding of how they will change with the environment. This study presents genomic data from this unique environment aged ∼20,000 to 1,000,000-years-old.

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Sipes K, Almatari AL, Eddie A, Williams D, Spirina E, Rivkina E, Liang R, Onstott TC, Vishnivetskaya T, Lloyd KG. Eight metagenome-assembled genomes provide evidence for microbial adaptation in 20,000 to 1,000,000-year-old Siberian permafrost. Applied and Environmental Microbiology. DOI: 10.1128/AEM.00972-21, in press.