TY - JOUR
T1 - Eight Metagenome-Assembled Genomes Provide Evidence for Microbial Adaptation in 20,000-to 1,000,000-Year-Old Siberian Permafrost
AU - Sipes, Katie
AU - Almatari, Abraham
AU - Eddie, Alexander
AU - Williams, Daniel
AU - Spirina, Elena
AU - Rivkina, Elizaveta
AU - Liang, Renxing
AU - Onstott, Tullis C.
AU - Vishnivetskaya, Tatiana A.
AU - Lloyda, Karen G.
N1 - Funding Information:
We thank Andrey Abramov, Nikita Demidov, Denis Shmelev, and Victor Sorokovikov from the Institute of Physicochemical and Biological Problems of Soil Science (Pushchino, Russia) for cooperation in the collection of permafrost samples. Peibo Li and Mackenzie Thorton helped extensively with microscopy. Nicholas T. Sipes helped with Python scripts; all in-house scripts are available at https://github.com/sipesk/SiberianMAGsPaper. This study was supported by the National Science Foundation (grants DEB-1442262 and DEB-1460058), the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program (grant DE-SC0020369), the Russian Government (assignment AAAA-A18-118013190181-6), and the Russian Foundation for Basic Research (grant 19-29-05003-mk).
Funding Information:
This study was supported by the National Science Foundation (grants DEB-1442262 and DEB-1460058), the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program (grant DE-SC0020369), the Russian Government (assignment AAAA-A18-118013190181-6), Basic Research (grant 19-29-05003-mk). We declare no conflicts of interests.
Publisher Copyright:
© 2021. American Society for Microbiology. All Rights Reserved.
PY - 2021/9
Y1 - 2021/9
N2 - Permafrost microbes may be metabolically active in microscopic layers of liquid brines, even in ancient soil. Metagenomics can help discern whether permafrost genomes (MAGs) were obtained from six depths (3.5 m to 20 m) of freshly cored permafrost from the Siberian 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 been obtained previously from nonpermafrost 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 greater proportions in the Clusters of Orthologous Groups (COGs) categories of energy production and conversion and carbohydrate transport and metabolism than did their nonpermafrost counterparts. They also contained genes for trehalose synthesis, thymine metabolism, mevalonate biosynthesis, and cellulose degradation, which were less prevalent in nonpermafrost 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 of high enough quality to assemble MAGs from microorganisms with adaptations to survive 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 under these extreme low-temperature and low-energy conditions. This will facilitate understanding how they will change with the environment. This study presents genomic data from this unique environment;20,000 to 1,000,000 years of age.
AB - Permafrost microbes may be metabolically active in microscopic layers of liquid brines, even in ancient soil. Metagenomics can help discern whether permafrost genomes (MAGs) were obtained from six depths (3.5 m to 20 m) of freshly cored permafrost from the Siberian 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 been obtained previously from nonpermafrost 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 greater proportions in the Clusters of Orthologous Groups (COGs) categories of energy production and conversion and carbohydrate transport and metabolism than did their nonpermafrost counterparts. They also contained genes for trehalose synthesis, thymine metabolism, mevalonate biosynthesis, and cellulose degradation, which were less prevalent in nonpermafrost 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 of high enough quality to assemble MAGs from microorganisms with adaptations to survive 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 under these extreme low-temperature and low-energy conditions. This will facilitate understanding how they will change with the environment. This study presents genomic data from this unique environment;20,000 to 1,000,000 years of age.
KW - MAGs
KW - bioinformatics
KW - environmental
KW - exobiology
KW - permafrost
UR - http://www.scopus.com/inward/record.url?scp=85116474818&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85116474818&partnerID=8YFLogxK
U2 - 10.1128/AEM.00972-21
DO - 10.1128/AEM.00972-21
M3 - Article
C2 - 34288700
AN - SCOPUS:85116474818
SN - 0099-2240
VL - 87
SP - 1
EP - 17
JO - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
IS - 19
ER -