DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Eight Metagenome-Assembled Genomes Provide Evidence for Microbial Adaptation in 20,000- to 1,000,000-Year-Old Siberian Permafrost

Abstract

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 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. Furthermore, 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 suggestmore » 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.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [2];  [3];  [3]; ORCiD logo [4]; ORCiD logo [1]
  1. Univ. of Tennessee, Knoxville, TN (United States)
  2. Institute of Physicochemical and Biological Problems of Soil Science, Pushchino (Russia)
  3. Princeton Univ., NJ (United States)
  4. Univ. of Tennessee, Knoxville, TN (United States); Institute of Physicochemical and Biological Problems of Soil Science, Pushchino (Russia)
Publication Date:
Research Org.:
Univ. of Tennessee, Knoxville, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Russian Foundation for Basic Research
OSTI Identifier:
1991903
Grant/Contract Number:  
SC0020369; DEB-1442262; DEB-1460058; 9-29-05003-mk
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 87; Journal Issue: 19; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; permafrost; MAGs; exobiology; environmental; bioinformatics

Citation Formats

Sipes, Katie, Almatari, Abraham, Eddie, Alexander, Williams, Daniel, Spirina, Elena, Rivkina, Elizaveta, Liang, Renxing, Onstott, Tullis C., Vishnivetskaya, Tatiana A., and Lloyd, Karen G. Eight Metagenome-Assembled Genomes Provide Evidence for Microbial Adaptation in 20,000- to 1,000,000-Year-Old Siberian Permafrost. United States: N. p., 2021. Web. doi:10.1128/aem.00972-21.
Sipes, Katie, Almatari, Abraham, Eddie, Alexander, Williams, Daniel, Spirina, Elena, Rivkina, Elizaveta, Liang, Renxing, Onstott, Tullis C., Vishnivetskaya, Tatiana A., & Lloyd, Karen G. Eight Metagenome-Assembled Genomes Provide Evidence for Microbial Adaptation in 20,000- to 1,000,000-Year-Old Siberian Permafrost. United States. https://doi.org/10.1128/aem.00972-21
Sipes, Katie, Almatari, Abraham, Eddie, Alexander, Williams, Daniel, Spirina, Elena, Rivkina, Elizaveta, Liang, Renxing, Onstott, Tullis C., Vishnivetskaya, Tatiana A., and Lloyd, Karen G. Fri . "Eight Metagenome-Assembled Genomes Provide Evidence for Microbial Adaptation in 20,000- to 1,000,000-Year-Old Siberian Permafrost". United States. https://doi.org/10.1128/aem.00972-21. https://www.osti.gov/servlets/purl/1991903.
@article{osti_1991903,
title = {Eight Metagenome-Assembled Genomes Provide Evidence for Microbial Adaptation in 20,000- to 1,000,000-Year-Old Siberian Permafrost},
author = {Sipes, Katie and Almatari, Abraham and Eddie, Alexander and Williams, Daniel and Spirina, Elena and Rivkina, Elizaveta and Liang, Renxing and Onstott, Tullis C. and Vishnivetskaya, Tatiana A. and Lloyd, Karen G.},
abstractNote = {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 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. Furthermore, 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.},
doi = {10.1128/aem.00972-21},
journal = {Applied and Environmental Microbiology},
number = 19,
volume = 87,
place = {United States},
year = {Fri Sep 10 00:00:00 EDT 2021},
month = {Fri Sep 10 00:00:00 EDT 2021}
}

Works referenced in this record:

Anvi’o: an advanced analysis and visualization platform for ‘omics data
journal, January 2015

  • Eren, A. Murat; Esen, Özcan C.; Quince, Christopher
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.1319

Preservation of frozen yeast cells by trehalose
journal, December 1999


Inhibition Experiments on Anaerobic Methane Oxidation
journal, October 1985


Cryoprotective properties of water in the Earth cryolithosphere and its role in exobiology
journal, February 1993

  • Gilichinsky, D. A.; Soina, V. S.; Petrova, M. A.
  • Origins of Life and Evolution of the Biosphere, Vol. 23, Issue 1
  • DOI: 10.1007/BF01581991

Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw
journal, November 2011

  • Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M.
  • Nature, Vol. 480, Issue 7377
  • DOI: 10.1038/nature10576

IMG/M: the integrated metagenome data management and comparative analysis system
journal, November 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Chu, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr975

Methane in Gas Shows from Boreholes in Epigenetic Permafrost of Siberian Arctic
journal, January 2019


Problems of the Cryogenic Soils’ Diagnostics in the Recent Russian Soil Classification System
journal, October 2019


Conservation of the metabolomic response to starvation across two divergent microbes
journal, December 2006

  • Brauer, M. J.; Yuan, J.; Bennett, B. D.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 51
  • DOI: 10.1073/pnas.0609508103

Supercooled Water Brines Within Permafrost—An Unknown Ecological Niche for Microorganisms: A Model for Astrobiology
journal, June 2003


Microbial diversity of active layer and permafrost in an acidic wetland from the Canadian High Arctic
journal, April 2011

  • Wilhelm, Roland C.; Niederberger, Thomas D.; Greer, Charles
  • Canadian Journal of Microbiology, Vol. 57, Issue 4
  • DOI: 10.1139/w11-004

The development of permafrost bacterial communities under submarine conditions
journal, July 2017

  • Mitzscherling, Julia; Winkel, Matthias; Winterfeld, Maria
  • Journal of Geophysical Research: Biogeosciences, Vol. 122, Issue 7
  • DOI: 10.1002/2017JG003859

Bacterial genome replication at subzero temperatures in permafrost
journal, August 2013

  • Tuorto, Steven J.; Darias, Phillip; McGuinness, Lora R.
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.140

Growth of Carnobacterium spp. from permafrost under low pressure, temperature, and anoxic atmosphere has implications for Earth microbes on Mars
journal, December 2012

  • Nicholson, W. L.; Krivushin, K.; Gilichinsky, D.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 2
  • DOI: 10.1073/pnas.1209793110

Microbial Populations in Antarctic Permafrost: Biodiversity, State, Age, and Implication for Astrobiology
journal, April 2007

  • Gilichinsky, D. A.; Wilson, G. S.; Friedmann, E. I.
  • Astrobiology, Vol. 7, Issue 2
  • DOI: 10.1089/ast.2006.0012

Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield
journal, March 2012


Predominance of Anaerobic, Spore-Forming Bacteria in Metabolically Active Microbial Communities from Ancient Siberian Permafrost
journal, May 2019

  • Liang, Renxing; Lau, Maggie; Vishnivetskaya, Tatiana
  • Applied and Environmental Microbiology, Vol. 85, Issue 15
  • DOI: 10.1128/AEM.00560-19

Changes in the Active, Dead, and Dormant Microbial Community Structure across a Pleistocene Permafrost Chronosequence
journal, January 2019

  • Burkert, Alexander; Douglas, Thomas A.; Waldrop, Mark P.
  • Applied and Environmental Microbiology, Vol. 85, Issue 7
  • DOI: 10.1128/AEM.02646-18

Reporting Key Features in Cold-Adapted Bacteria
journal, March 2018


Phylogenomic reconstruction of archaeal fatty acid metabolism: Fatty acid metabolism in archaea
journal, January 2014

  • Dibrova, Daria V.; Galperin, Michael Y.; Mulkidjanian, Armen Y.
  • Environmental Microbiology, Vol. 16, Issue 4
  • DOI: 10.1111/1462-2920.12359

Staphylococcus aureus Mevalonate Kinase: Isolation and Characterization of an Enzyme of the Isoprenoid Biosynthetic Pathway
journal, January 2004


Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Phylogenetic Characterization of Marine Benthic Archaea in Organic-Poor Sediments of the Eastern Equatorial Pacific Ocean (ODP Site 1225)
journal, September 2016


Isotope-Ratio and Background Corrections for Accelerator Mass Spectrometry Radiocarbon Measurements
journal, January 1990


Biodiversity of cryopegs in permafrost
journal, June 2005


Genomic and transcriptomic insights into the ecology and metabolism of benthic archaeal cosmopolitan, Thermoprofundales (MBG-D archaea)
journal, December 2018


Recovery and phylogenetic analysis of archaeal rRNA sequences from continental shelf sediments
journal, April 1998


A proteomic analysis ofPsychrobacter articus 273-4 adaptation to low temperature and salinity using a 2-D liquid mapping approach
journal, February 2007

  • Zheng, Suping; Ponder, Monica A.; Shih, Janice Yang Jen
  • ELECTROPHORESIS, Vol. 28, Issue 3
  • DOI: 10.1002/elps.200600173

metaSPAdes: a new versatile metagenomic assembler
journal, March 2017

  • Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton
  • Genome Research, Vol. 27, Issue 5
  • DOI: 10.1101/gr.213959.116

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Inter-laboratory quantification of Bacteria and Archaea in deeply buried sediments of the Baltic Sea (IODP Expedition 347)
journal, January 2017

  • Buongiorno, Joy; Turner, Stephanie; Webster, Gordon
  • FEMS Microbiology Ecology
  • DOI: 10.1093/femsec/fix007

Global Patterns of Abundance, Diversity and Community Structure of the Aminicenantes (Candidate Phylum OP8)
journal, March 2014


Biosynthesis of Isoprenoids: Crystal Structure of the [4Fe–4S] Cluster Protein IspG
journal, December 2010

  • Lee, Matthias; Gräwert, Tobias; Quitterer, Felix
  • Journal of Molecular Biology, Vol. 404, Issue 4
  • DOI: 10.1016/j.jmb.2010.09.050

MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015


A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
journal, August 2018

  • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
  • Nature Biotechnology, Vol. 36, Issue 10
  • DOI: 10.1038/nbt.4229

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Bacterial growth at −15 °C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1
journal, February 2013

  • Mykytczuk, Nadia C. S.; Foote, Simon J.; Omelon, Chris R.
  • The ISME Journal, Vol. 7, Issue 6
  • DOI: 10.1038/ismej.2013.8

The COG database: a tool for genome-scale analysis of protein functions and evolution
journal, January 2000


Hydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres
journal, April 2020

  • Chakraborty, Anirban; Ruff, S. Emil; Dong, Xiyang
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 20
  • DOI: 10.1073/pnas.2002289117

Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

Physiological roles of trehalose in bacteria and yeasts: a comparative analysis
journal, September 2000


Genome-centric view of carbon processing in thawing permafrost
journal, July 2018


Cellobiose phosphorylase (EC 2.4.1.20) of Cellulomonas: occurrence, induction, and its role in cellobiose metabolism
journal, September 1983

  • Schimz, Karl. -L.; Broll, Birgitt; John, Birgit
  • Archives of Microbiology, Vol. 135, Issue 4
  • DOI: 10.1007/BF00413475

Isolation of nucleic acids and cultures from fossil ice and permafrost
journal, March 2004

  • Willerslev, Eske; Hansen, Anders J.; Poinar, Hendrik N.
  • Trends in Ecology & Evolution, Vol. 19, Issue 3
  • DOI: 10.1016/j.tree.2003.11.010

The Structure of Resting Bacterial Populations in Soil and Subsoil Permafrost
journal, September 2004

  • Soina, Vera S.; Mulyukin, Andrei L.; Demkina, Elena V.
  • Astrobiology, Vol. 4, Issue 3
  • DOI: 10.1089/ast.2004.4.345

The Genome Sequence of Psychrobacter arcticus 273-4, a Psychroactive Siberian Permafrost Bacterium, Reveals Mechanisms for Adaptation to Low-Temperature Growth
journal, February 2010

  • Ayala-del-Rio, H. L.; Chain, P. S.; Grzymski, J. J.
  • Applied and Environmental Microbiology, Vol. 76, Issue 7
  • DOI: 10.1128/AEM.02101-09

Preservation of cell structures in permafrost: A model for exobiology
journal, March 1995


Low-temperature recovery strategies for the isolation of bacteria from ancient permafrost sediments
journal, June 2000

  • Vishnivetskaya, Tatiana; Kathariou, Sophia; McGrath, John
  • Extremophiles, Vol. 4, Issue 3
  • DOI: 10.1007/s007920070031

Methanogens in the Antarctic Dry Valley permafrost
journal, June 2018

  • Vishnivetskaya, Tatiana A.; Buongiorno, Joy; Bird, Jordan
  • FEMS Microbiology Ecology, Vol. 94, Issue 8
  • DOI: 10.1093/femsec/fiy109

KBase: The United States Department of Energy Systems Biology Knowledgebase
journal, July 2018

  • Arkin, Adam P.; Cottingham, Robert W.; Henry, Christopher S.
  • Nature Biotechnology, Vol. 36, Issue 7
  • DOI: 10.1038/nbt.4163

Ice Nucleation and the Substrate-ice Interface
journal, November 1967


Quantitative colorimetric measurement of cellulose degradation under microbial culture conditions
journal, March 2012

  • Haft, Rembrandt J. F.; Gardner, Jeffrey G.; Keating, David H.
  • Applied Microbiology and Biotechnology, Vol. 94, Issue 1
  • DOI: 10.1007/s00253-012-3968-5

Metagenomic analyses of the late Pleistocene permafrost – additional tools for reconstruction of environmental conditions
journal, January 2016

  • Rivkina, Elizaveta; Petrovskaya, Lada; Vishnivetskaya, Tatiana
  • Biogeosciences, Vol. 13, Issue 7
  • DOI: 10.5194/bg-13-2207-2016

Are permafrost microorganisms as old as permafrost?
journal, February 2021

  • Abramov, Andrey; Vishnivetskaya, Tatiana; Rivkina, Elizaveta
  • FEMS Microbiology Ecology, Vol. 97, Issue 2
  • DOI: 10.1093/femsec/fiaa260

Bacterial Community in Ancient Siberian Permafrost as Characterized by Culture and Culture-Independent Methods
journal, June 2006

  • Vishnivetskaya, Tatiana A.; Petrova, Maya A.; Urbance, John
  • Astrobiology, Vol. 6, Issue 3
  • DOI: 10.1089/ast.2006.6.400

Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes
journal, September 2018


Caloric Restriction Extends Yeast Chronological Lifespan by Altering a Pattern of Age-Related Changes in Trehalose Concentration
journal, January 2012


A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction
journal, April 2018


Uncultured Microbial Phyla Suggest Mechanisms for Multi-Thousand-Year Subsistence in Baltic Sea Sediments
journal, April 2019


The microbial ecology of permafrost
journal, May 2014

  • Jansson, Janet K.; Taş, Neslihan
  • Nature Reviews Microbiology, Vol. 12, Issue 6
  • DOI: 10.1038/nrmicro3262

Microbial survival strategies in ancient permafrost: insights from metagenomics
journal, July 2017

  • Mackelprang, Rachel; Burkert, Alexander; Haw, Monica
  • The ISME Journal, Vol. 11, Issue 10
  • DOI: 10.1038/ismej.2017.93

Phylogenetic Analysis of Anaerobic Psychrophilic Enrichment Cultures Obtained from a Greenland Glacier Ice Core
journal, April 2003


Characterization of the Prokaryotic Diversity in Cold Saline Perennial Springs of the Canadian High Arctic
journal, March 2007

  • Perreault, Nancy N.; Andersen, Dale T.; Pollard, Wayne H.
  • Applied and Environmental Microbiology, Vol. 73, Issue 5
  • DOI: 10.1128/AEM.01729-06

Ancient bacteria show evidence of DNA repair
journal, August 2007

  • Johnson, S. S.; Hebsgaard, M. B.; Christensen, T. R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 36
  • DOI: 10.1073/pnas.0706787104

Metagenomics uncovers gaps in amplicon-based detection of microbial diversity
journal, February 2016


Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles
journal, July 2017

  • Stepanauskas, Ramunas; Fergusson, Elizabeth A.; Brown, Joseph
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-00128-z

Modern tundra landscapes of the Kolyma Lowland and their evolution in the Holocene
journal, October 2009

  • Veremeeva, Alexandra; Gubin, Stanislav
  • Permafrost and Periglacial Processes, Vol. 20, Issue 4
  • DOI: 10.1002/ppp.674

Exobiological aspects of mass transfer in microzones of permafrost deposits
journal, January 1996


Two Metagenomes from Late Pleistocene Northeast Siberian Permafrost
journal, February 2015

  • Krivushin, Kirill; Kondrashov, Fyodor; Shmakova, Lyubov
  • Genome Announcements, Vol. 3, Issue 1
  • DOI: 10.1128/genomeA.01380-14

Overcoming inefficient cellobiose fermentation by cellobiose phosphorylase in the presence of xylose
journal, January 2014

  • Chomvong, Kulika; Kordić, Vesna; Li, Xin
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/1754-6834-7-85

Metagenome-assembled genome distribution and key functionality highlight importance of aerobic metabolism in Svalbard permafrost
journal, April 2020

  • Xue, Yaxin; Jonassen, Inge; Øvreås, Lise
  • FEMS Microbiology Ecology, Vol. 96, Issue 5
  • DOI: 10.1093/femsec/fiaa057

Sedimentary characteristics and origin of the Late Pleistocene Ice Complex on north-east Siberian Arctic coastal lowlands and islands – A review
journal, August 2011


The growing tree of Archaea: new perspectives on their diversity, evolution and ecology
journal, August 2017

  • Adam, Panagiotis S.; Borrel, Guillaume; Brochier-Armanet, Céline
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.122

Potential for primary productivity in a globally-distributed bacterial phototroph
journal, March 2018


A large-scale evaluation of algorithms to calculate average nucleotide identity
journal, February 2017


Temperature dependence of metabolic rates for microbial growth, maintenance, and survival
journal, March 2004

  • Price, P. B.; Sowers, T.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 13
  • DOI: 10.1073/pnas.0400522101

Predominant archaea in marine sediments degrade detrital proteins
journal, March 2013

  • Lloyd, Karen G.; Schreiber, Lars; Petersen, Dorthe G.
  • Nature, Vol. 496, Issue 7444
  • DOI: 10.1038/nature12033

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Deep Yedoma permafrost: A synthesis of depositional characteristics and carbon vulnerability
journal, September 2017


Bacteria primarily metabolize at the active layer/permafrost border in the peat core from a permafrost region in western Siberia
journal, February 2017


Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper-arid polar desert: Ecology of Dry Valley permafrost and cryptoendoliths
journal, June 2016

  • Goordial, Jacqueline; Davila, Alfonso; Greer, Charles W.
  • Environmental Microbiology, Vol. 19, Issue 2
  • DOI: 10.1111/1462-2920.13353

Identification, Evolution, and Essentiality of the Mevalonate Pathway for Isopentenyl Diphosphate Biosynthesis in Gram-Positive Cocci
journal, August 2000


Stratification of Archaea in the Deep Sediments of a Freshwater Meromictic Lake: Vertical Shift from Methanogenic to Uncultured Archaeal Lineages
journal, August 2012


Biosynthesis of Isoprenoids via Mevalonate in Archaea: The Lost Pathway
journal, October 2000

  • Smit, Arian; Mushegian, Arcady
  • Genome Research, Vol. 10, Issue 10
  • DOI: 10.1101/gr.145600