Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes

Saw, Jimmy H.; Spang, Anja; Zaremba-Niedzwiedzka, Katarzyna; Juzokaite, Lina; Dodsworth, Jeremy A.; Murugapiran, Senthil K.; Colman, Dan R.; Takacs-Vesbach, Cristina; Hedlund, Brian P.; Guy, Lionel; Ettema, Thijs J. G.

doi:10.1098/rstb.2014.0328

Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes

Journal Article · Mon Aug 31 00:00:00 EDT 2015 · Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences

DOI:https://doi.org/10.1098/rstb.2014.0328· OSTI ID:1343570

Saw, Jimmy H. ^[1]; Spang, Anja ^[2]; Zaremba-Niedzwiedzka, Katarzyna ^[2]; Juzokaite, Lina ^[2]; Dodsworth, Jeremy A. ^[3]; Murugapiran, Senthil K. ^[4]; Colman, Dan R. ^[5]; Takacs-Vesbach, Cristina ^[5]; Hedlund, Brian P. ^[6]; Guy, Lionel ^[2]; Ettema, Thijs J. G. ^[2]

Uppsala Univ., Uppsala (Sweden); DOE Office of Scientific and Technical Information (OSTI)
Uppsala Univ., Uppsala (Sweden)
Univ. of Nevada, Las Vegas, NV (United States); California State Univ. (CalState), San Bernardino, CA (United States)
Univ. of Nevada, Las Vegas, NV (United States)
Univ. of New Mexico, Albuquerque, NM (United States)
Univ. of Nevada, Las Vegas, NV (United States). School of Life Sciences

The origin of eukaryotes represents an enigmatic puzzle, which is still lacking a number of essential pieces. Whereas it is currently accepted that the process of eukaryogenesis involved an interplay between a host cell and an alphaproteobacterial endosymbiont, we currently lack detailed information regarding the identity and nature of these players. A number of studies have provided increasing support for the emergence of the eukaryotic host cell from within the archaeal domain of life, displaying a specific affiliation with the archaeal TACK superphylum. Recent studies have shown that genomic exploration of yet-uncultivated archaea, the so-called archaeal 'dark matter', is able to provide unprecedented insights into the process of eukaryogenesis. Here, we provide an overview of state-of-the-art cultivation-independent approaches, and demonstrate how these methods were used to obtain draft genome sequences of several novel members of the TACK superphylum, including Lokiarchaeum, two representatives of the Miscellaneous Crenarchaeotal Group (Bathyarchaeota), and a Korarchaeum-related lineage. In conclusion, the maturation of cultivation-independent genomics approaches, as well as future developments in next-generation sequencing technologies, will revolutionize our current view of microbial evolution and diversity, and provide profound new insights into the early evolution of life, including the enigmatic origin of the eukaryotic cell.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Nevada, Las Vegas, NV (United States)

Sponsoring Organization:: ERC; EU; Marie Curie; NASA; NSF; Swedish Research Council; USDOE

Grant/Contract Number:: EE0000716; SC0006771

OSTI ID:: 1343570

Journal Information:: Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, Journal Name: Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences Journal Issue: 1678 Vol. 370; ISSN 0962-8436

Publisher:: The Royal Society PublishingCopyright Statement

Country of Publication:: United States

Language:: English

References (87)

Binning Metagenomic Contigs Using Unsupervised Clustering and Reference Databases Jiang, Zhongjun; Li, Xiaobo; Guo, Lijun Interdisciplinary Sciences: Computational Life Sciences, Vol. 14, Issue 4 https://doi.org/10.1007/s12539-022-00526-y	journal	May 2022
Single cell genomics: an individual look at microbes Stepanauskas, Ramunas Current Opinion in Microbiology, Vol. 15, Issue 5 https://doi.org/10.1016/j.mib.2012.09.001	journal	October 2012
Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis Poole, Anthony M.; Neumann, Nadja Research in Microbiology, Vol. 162, Issue 1 https://doi.org/10.1016/j.resmic.2010.10.002	journal	January 2011
Ancestral lipid biosynthesis and early membrane evolution Peretó, Juli; López-García, Purificación; Moreira, David Trends in Biochemical Sciences, Vol. 29, Issue 9 https://doi.org/10.1016/j.tibs.2004.07.002	journal	September 2004
Supertrees and symbiosis in eukaryote genome evolution Esser, Christian; Martin, William Trends in Microbiology, Vol. 15, Issue 10 https://doi.org/10.1016/j.tim.2007.09.001	journal	October 2007
Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses Meng, Jun; Xu, Jun; Qin, Dan The ISME Journal, Vol. 8, Issue 3 https://doi.org/10.1038/ismej.2013.174	journal	October 2013
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
Eukaryotic evolution, changes and challenges Embley, T. Martin; Martin, William Nature, Vol. 440, Issue 7084 https://doi.org/10.1038/nature04546	journal	March 2006
Predominant archaea in marine sediments degrade detrital proteins Lloyd, Karen G.; Schreiber, Lars; Petersen, Dorthe G. Nature, Vol. 496, Issue 7444 https://doi.org/10.1038/nature12033	journal	March 2013
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
An archaeal origin of eukaryotes supports only two primary domains of life Williams, Tom A.; Foster, Peter G.; Cox, Cymon J. Nature, Vol. 504, Issue 7479 https://doi.org/10.1038/nature12779	journal	December 2013
Complex archaea that bridge the gap between prokaryotes and eukaryotes Spang, Anja; Saw, Jimmy H.; Jørgensen, Steffen L. Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14447	journal	May 2015
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam Nature Biotechnology, Vol. 31, Issue 6 https://doi.org/10.1038/nbt.2579	journal	May 2013
Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge Pedersen, Rolf B.; Rapp, Hans Tore; Thorseth, Ingunn H. Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1124	journal	November 2010
Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models Brady, Arthur; Salzberg, Steven L. Nature Methods, Vol. 6, Issue 9 https://doi.org/10.1038/nmeth.1358	journal	August 2009
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
PhymmBL expanded: confidence scores, custom databases, parallelization and more Brady, Arthur; Salzberg, Steven Nature Methods, Vol. 8, Issue 5 https://doi.org/10.1038/nmeth0511-367	journal	April 2011
Accurate phylogenetic classification of variable-length DNA fragments McHardy, Alice Carolyn; Martín, Héctor García; Tsirigos, Aristotelis Nature Methods, Vol. 4, Issue 1 https://doi.org/10.1038/nmeth976	journal	December 2006
Archaeal genetics — the third way Allers, Thorsten; Mevarech, Moshe Nature Reviews Genetics, Vol. 6, Issue 1 https://doi.org/10.1038/nrg1504	journal	January 2005
Recent advances in genomic DNA sequencing of microbial species from single cells Lasken, Roger S.; McLean, Jeffrey S. Nature Reviews Genetics, Vol. 15, Issue 9 https://doi.org/10.1038/nrg3785	journal	August 2014
The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Gribaldo, Simonetta; Poole, Anthony M.; Daubin, Vincent Nature Reviews Microbiology, Vol. 8, Issue 10 https://doi.org/10.1038/nrmicro2426	journal	September 2010
From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell Martijn, Joran; Ettema, Thijs J. G. Biochemical Society Transactions, Vol. 41, Issue 1 https://doi.org/10.1042/bst20120292	journal	January 2013
Archaeal chromatin and transcription: Chromatin and transcription Reeve, John N. Molecular Microbiology, Vol. 48, Issue 3 https://doi.org/10.1046/j.1365-2958.2003.03439.x	journal	April 2003
From The Cover: Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem Spear, J. R.; Walker, J. J.; McCollom, T. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7, p. 2555-2560 https://doi.org/10.1073/pnas.0409574102	journal	January 2005
The global phylogeny of glycolytic enzymes Canback, B.; Andersson, S. G. E.; Kurland, C. G. Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.082112499	journal	April 2002
Microbiology in transition. Woese, C. R. Proceedings of the National Academy of Sciences, Vol. 91, Issue 5 https://doi.org/10.1073/pnas.91.5.1601	journal	March 1994
Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Barns, S. M.; Delwiche, C. F.; Palmer, J. D. Proceedings of the National Academy of Sciences, Vol. 93, Issue 17 https://doi.org/10.1073/pnas.93.17.9188	journal	August 1996
Genomic evidence for two functionally distinct gene classes Rivera, M. C.; Jain, R.; Moore, J. E. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.6239	journal	May 1998
MetaCluster 4.0: A Novel Binning Algorithm for NGS Reads and Huge Number of Species Wang, Yi; Leung, Henry C. M.; Yiu, S. M. Journal of Computational Biology, Vol. 19, Issue 2 https://doi.org/10.1089/cmb.2011.0276	journal	February 2012
Current opportunities and challenges in microbial metagenome analysis--a bioinformatic perspective Teeling, H.; Glockner, F. O. Briefings in Bioinformatics, Vol. 13, Issue 6 https://doi.org/10.1093/bib/bbs039	journal	September 2012
An Evolutionary Network of Genes Present in the Eukaryote Common Ancestor Polls Genomes on Eukaryotic and Mitochondrial Origin Thiergart, Thorsten; Landan, Giddy; Schenk, Marc Genome Biology and Evolution, Vol. 4, Issue 4 https://doi.org/10.1093/gbe/evs018	journal	January 2012
Supertrees Disentangle the Chimerical Origin of Eukaryotic Genomes Pisani, Davide; Cotton, James A.; McInerney, James O. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm095	journal	May 2007
Phylogenomic Test of the Hypotheses for the Evolutionary Origin of Eukaryotes Rochette, Nicolas C.; Brochier-Armanet, Céline; Gouy, Manolo Molecular Biology and Evolution, Vol. 31, Issue 4 https://doi.org/10.1093/molbev/mst272	journal	January 2014
Phylogenetic classification of short environmental DNA fragments Krause, Lutz; Diaz, Naryttza N.; Goesmann, Alexander Nucleic Acids Research, Vol. 36, Issue 7 https://doi.org/10.1093/nar/gkn038	journal	February 2008
Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group Nunoura, Takuro; Takaki, Yoshihiro; Kakuta, Jungo Nucleic Acids Research, Vol. 39, Issue 8 https://doi.org/10.1093/nar/gkq1228	journal	December 2010
A congruent phylogenomic signal places eukaryotes within the Archaea Williams, Tom A.; Foster, Peter G.; Nye, Tom M. W. Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1749 https://doi.org/10.1098/rspb.2012.1795	journal	October 2012
The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes Koonin, E. V.; Yutin, N. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 4 https://doi.org/10.1101/cshperspect.a016188	journal	April 2014
Transcript amplification from single bacterium for transcriptome analysis Kang, Y.; Norris, M. H.; Zarzycki-Siek, J. Genome Research, Vol. 21, Issue 6 https://doi.org/10.1101/gr.116103.110	journal	May 2011
MEGAN analysis of metagenomic data Huson, D. H.; Auch, A. F.; Qi, J. Genome Research, Vol. 17, Issue 3 https://doi.org/10.1101/gr.5969107	journal	February 2007
Genomes from Metagenomics Sharon, I.; Banfield, J. F. Science, Vol. 342, Issue 6162 https://doi.org/10.1126/science.1247023	journal	November 2013
Omic Approaches in Microbial Ecology: Charting the Unknown: Analysis of whole-community sequence data is unveiling the diversity and function of specific microbial groups within uncultured phyla and across entire microbial ecosystems Dick, Gregory J.; Baker, Brett J. Microbe Magazine, Vol. 8, Issue 9 https://doi.org/10.1128/microbe.8.353.1	journal	September 2013
Metagenomics: Application of Genomics to Uncultured Microorganisms Handelsman, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 4 https://doi.org/10.1128/mmbr.68.4.669-685.2004	journal	December 2004
Microfluidics Expanding the Frontiers of Microbial Ecology Rusconi, Roberto; Garren, Melissa; Stocker, Roman Annual Review of Biophysics, Vol. 43, Issue 1 https://doi.org/10.1146/annurev-biophys-051013-022916	journal	May 2014
The Common Ancestor of Archaea and Eukarya Was Not an Archaeon Forterre, Patrick Archaea, Vol. 2013 https://doi.org/10.1155/2013/372396	journal	January 2013
A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya Brochier-Armanet, Céline; Gribaldo, Simonetta; Forterre, Patrick Biology Direct, Vol. 3, Issue 1 https://doi.org/10.1186/1745-6150-3-54	journal	January 2008
Archaeal origin of tubulin Yutin, Natalya; Koonin, Eugene V. Biology Direct, Vol. 7, Issue 1 https://doi.org/10.1186/1745-6150-7-10	journal	January 2012
MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm Wu, Yu-Wei; Tang, Yung-Hsu; Tringe, Susannah G. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-26	journal	August 2014
Community-wide analysis of microbial genome sequence signatures Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J. Genome Biology, Vol. 10, Issue 8 https://doi.org/10.1186/gb-2009-10-8-r85	journal	January 2009
The origin and early evolution of eukaryotes in the light of phylogenomics Koonin, Eugene V. Genome Biology, Vol. 11, Issue 5 https://doi.org/10.1186/gb-2010-11-5-209	journal	January 2010
Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis Blainey, Paul C.; Mosier, Annika C.; Potanina, Anastasia PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016626	journal	February 2011
An Overview of Endosymbiotic Models for the Origins of Eukaryotes, Their ATP-Producing Organelles (Mitochondria and Hydrogenosomes), and Their Heterotrophic Lifestyle Martin, William; Hoffmeister, Meike; Rotte, Carmen Biological Chemistry, Vol. 382, Issue 11 https://doi.org/10.1515/bc.2001.187	journal	January 2001
Archaea in Organic-Lean and Organic-Rich Marine Subsurface Sediments: An Environmental Gradient Reflected in Distinct Phylogenetic Lineages Durbin, Alan M.; Teske, Andreas Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00168	journal	January 2012
Reconstructing each cell's genome within complex microbial communitiesâ€”dream or reality? Clingenpeel, Scott; Clum, Alicia; Schwientek, Patrick Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00771	journal	January 2015
ClaMS: A Classifier for Metagenomic Sequences Pati, Amrita; Heath, Lenwood S.; Kyrpides, Nikos C. Standards in Genomic Sciences, Vol. 5, Issue 2 https://doi.org/10.4056/sigs.2075298	journal	November 2011
An archaeal origin for the actin cytoskeleton: Implications for eukaryogenesis Bernander, Rolf; Lind, Anders E.; Ettema, Thijs J. G. Communicative & Integrative Biology, Vol. 4, Issue 6 https://doi.org/10.4161/cib.16974	journal	November 2011
Data from: Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes Saw, J. H.; Sprang, A.; Zaremba-Niedzwiedzka, K. Dryad, 821.0 Kb https://doi.org/10.5061/dryad.df264	dataset	December 2015
PhyloPythiaS+ : a self-training method for the rapid reconstruction of low-ranking taxonomic bins from metagenomes Gregor, Ivan; Dröge, Johannes; Schirmer, Melanie PeerJ, Vol. 4 https://doi.org/10.7717/peerj.1603	journal	January 2016
Nucleotide sequence of pig plasma gelsolin Way, Michael; Weeds, Alan Journal of Molecular Biology, Vol. 203, Issue 4 https://doi.org/10.1016/0022-2836(88)90132-5	journal	October 1988
Remarkable archaeal diversity detected in a Yellowstone national park hot spring environment Barns, S. M.; Fundgya, R. E.; Jeffries, M. W. Trends in Genetics, Vol. 10, Issue 6 https://doi.org/10.1016/0168-9525(94)90248-8	journal	June 1994
Archaebacteria (Archaea) and the origin of the eukaryotic nucleus Martin, William Current Opinion in Microbiology, Vol. 8, Issue 6 https://doi.org/10.1016/j.mib.2005.10.004	journal	December 2005
The archaeal ‘TACK’ superphylum and the origin of eukaryotes Guy, Lionel; Ettema, Thijs J. G. Trends in Microbiology, Vol. 19, Issue 12 https://doi.org/10.1016/j.tim.2011.09.002	journal	December 2011
Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments Kubo, Kyoko; Lloyd, Karen G.; F. Biddle, Jennifer The ISME Journal, Vol. 6, Issue 10 https://doi.org/10.1038/ismej.2012.37	journal	May 2012
Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage Dodsworth, Jeremy A.; Blainey, Paul C.; Murugapiran, Senthil K. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2884	journal	May 2013
From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell Martijn, Joran; Ettema, Thijs J. G. Biochemical Society Transactions, Vol. 41, Issue 1 https://doi.org/10.1042/BST20120292	journal	January 2013
Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth Marcy, Y.; Ouverney, C.; Bik, E. M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 29, p. 11889-11894 https://doi.org/10.1073/pnas.0704662104	journal	July 2007
A unique cell division machinery in the Archaea Lindas, A. -C.; Karlsson, E. A.; Lindgren, M. T. Proceedings of the National Academy of Sciences, Vol. 105, Issue 48 https://doi.org/10.1073/pnas.0809467105	journal	November 2008
Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Barns, S. M.; Fundyga, R. E.; Jeffries, M. W. Proceedings of the National Academy of Sciences, Vol. 91, Issue 5 https://doi.org/10.1073/pnas.91.5.1609	journal	March 1994
The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Cavalier-Smith, T. International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 2 https://doi.org/10.1099/00207713-52-2-297	journal	March 2002
The Archaeal Legacy of Eukaryotes: A Phylogenomic Perspective Guy, L.; Saw, J. H.; Ettema, T. J. G. Cold Spring Harbor Perspectives in Biology, Vol. 6, Issue 10 https://doi.org/10.1101/cshperspect.a016022	journal	July 2014
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization Sharon, I.; Morowitz, M. J.; Thomas, B. C. Genome Research, Vol. 23, Issue 1 https://doi.org/10.1101/gr.142315.112	journal	August 2012
An actin-based cytoskeleton in archaea: An archaeal cytoskeleton Ettema, Thijs J. G.; Lindås, Ann-Christin; Bernander, Rolf Molecular Microbiology, Vol. 80, Issue 4 https://doi.org/10.1111/j.1365-2958.2011.07635.x	journal	April 2011
A Role for the ESCRT System in Cell Division in Archaea Samson, R. Y.; Obita, T.; Freund, S. M. Science, Vol. 322, Issue 5908 https://doi.org/10.1126/science.1165322	journal	December 2008
Ecology of Sulfur-Oxidizing Bacteria in Hot Acid Soils Fliermans, Carl B.; Brock, Thomas D. Journal of Bacteriology, Vol. 111, Issue 2 https://doi.org/10.1128/JB.111.2.343-350.1972	journal	January 1972
Metagenomics: Application of Genomics to Uncultured Microorganisms Handelsman, J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 4 https://doi.org/10.1128/MMBR.68.4.669-685.2004	journal	December 2004
Metagenomics: Application of Genomics to Uncultured Microorganisms Handelsman, Jo Microbiology and Molecular Biology Reviews, Vol. 69, Issue 1 https://doi.org/10.1128/mmbr.69.1.195.2005	journal	March 2005
Genomic Analysis at the Single-Cell Level Kalisky, Tomer; Blainey, Paul; Quake, Stephen R. Annual Review of Genetics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-genet-102209-163607	journal	December 2011
Orthologs of the small RPB8 subunit of the eukaryotic RNA polymerases are conserved in hyperthermophilic Crenarchaeota and "Korarchaeota" Koonin, Eugene V.; Makarova, Kira S.; Elkins, James G. Biology Direct, Vol. 2, Issue 1 https://doi.org/10.1186/1745-6150-2-38	journal	January 2007
The origins of phagocytosis and eukaryogenesis Yutin, Natalya; Wolf, Maxim Y.; Wolf, Yuri I. Biology Direct, Vol. 4, Issue 1 https://doi.org/10.1186/1745-6150-4-9	journal	January 2009
Assembling the Marine Metagenome, One Cell at a Time Woyke, Tanja; Xie, Gary; Copeland, Alex PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005299	journal	April 2009
Korarchaeota Diversity, Biogeography, and Abundance in Yellowstone and Great Basin Hot Springs and Ecological Niche Modeling Based on Machine Learning Miller-Coleman, Robin L.; Dodsworth, Jeremy A.; Ross, Christian A. PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0035964	journal	May 2012
The PhyloPythiaS Web Server for Taxonomic Assignment of Metagenome Sequences Patil, Kaustubh Raosaheb; Roune, Linus; McHardy, Alice Carolyn PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0038581	journal	June 2012
An Overview of Endosymbiotic Models for the Origins of Eukaryotes, Their ATP-Producing Organelles (Mitochondria and Hydrogenosomes), and Their Heterotrophic Lifestyle Martin, William; Hoffmeister, Meike; Rotte, Carmen Biological Chemistry, Vol. 382, Issue 11 https://doi.org/10.1515/BC.2001.187	journal	January 2001
Archaea in Organic-Lean and Organic-Rich Marine Subsurface Sediments: An Environmental Gradient Reflected in Distinct Phylogenetic Lineages Andreas, Teske,; M., Durbin, Alan The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/t8y0-as16	text	January 2012
The Binning of Metagenomic Contigs for Microbial Physiology of Mixed Cultures Strous, Marc; Kraft, Beate; Bisdorf, Regina Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00410	journal	January 2012
Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge Pedersen, Rolf B.; Rapp, Hans T.; Thorseth, Ingunn H. ETH Zurich https://doi.org/10.3929/ethz-b-000028475	text	January 2010
Cell division and the ESCRT complex: A surprise from the Archaea Ettema, Thijs J. G.; Bernander, Rolf Communicative & Integrative Biology, Vol. 2, Issue 2 https://doi.org/10.4161/cib.7523	journal	March 2009
GroopM: an automated tool for the recovery of population genomes from related metagenomes Imelfort, Michael; Parks, Donovan; Woodcroft, Ben J. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.603	journal	January 2014

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Changing ideas about eukaryotic origins Williams, Tom A.; Embley, T. Martin Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1678 https://doi.org/10.1098/rstb.2014.0318	journal	September 2015
Assessing the viral content of uncultured picoeukaryotes in the global‐ocean by single cell genomics Castillo, Yaiza M.; Mangot, Jean‐François; Benites, Luiz Felipe Molecular Ecology, Vol. 28, Issue 18 https://doi.org/10.1111/mec.15210	journal	September 2019
The Physiology of Phagocytosis in the Context of Mitochondrial Origin Martin, William F.; Tielens, Aloysius G. M.; Mentel, Marek Microbiology and Molecular Biology Reviews, Vol. 81, Issue 3 https://doi.org/10.1128/mmbr.00008-17	journal	June 2017
Birth of Archaeal Cells: Molecular Phylogenetic Analyses of G1P Dehydrogenase, G3P Dehydrogenases, and Glycerol Kinase Suggest Derived Features of Archaeal Membranes Having G1P Polar Lipids Yokobori, Shin-ichi; Nakajima, Yoshiki; Akanuma, Satoshi Archaea, Vol. 2016 https://doi.org/10.1155/2016/1802675	journal	January 2016
Microbial Community Response to Simulated Petroleum Seepage in Caspian Sea Sediments Stagars, Marion H.; Mishra, Sonakshi; Treude, Tina Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00764	journal	April 2017
Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland Daebeler, Anne; Herbold, Craig W.; Vierheilig, Julia Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00193	journal	February 2018

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