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

Journal Article · · Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
 [1];  [1];  [1];  [1];  [2];  [3];  [4];  [4];  [5];  [1];  [1]
  1. Uppsala Univ., Uppsala (Sweden)
  2. Univ. of Nevada, Las Vegas, NV (United States); California State Univ. (CalState), San Bernardino, CA (United States)
  3. Univ. of Nevada, Las Vegas, NV (United States)
  4. Univ. of New Mexico, Albuquerque, NM (United States)
  5. 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.

Research Organization:
Univ. of Nevada, Las Vegas, NV (United States)
Sponsoring Organization:
USDOE; National Aeronautics and Space Administration (NASA); National Science Foundation (NSF); EU; ERC; Swedish Research Council (SRC); Marie Curie
Grant/Contract Number:
SC0006771; EE-0000716; EXO-NNX11AR78G; 621-2009-4813
OSTI ID:
1343570
Journal Information:
Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences, Vol. 370, Issue 1678; ISSN 0962-8436
Publisher:
The Royal Society PublishingCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 30 works
Citation information provided by
Web of Science

References (84)

MetaCluster 4.0: A Novel Binning Algorithm for NGS Reads and Huge Number of Species journal February 2012
ClaMS: A Classifier for Metagenomic Sequences journal November 2011
The Binning of Metagenomic Contigs for Microbial Physiology of Mixed Cultures journal January 2012
A congruent phylogenomic signal places eukaryotes within the Archaea journal October 2012
PhymmBL expanded: confidence scores, custom databases, parallelization and more journal April 2011
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization journal August 2012
The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. journal March 2002
Community-wide analysis of microbial genome sequence signatures journal January 2009
The archaeal ‘TACK’ superphylum and the origin of eukaryotes journal December 2011
Ancestral lipid biosynthesis and early membrane evolution journal September 2004
Cell division and the ESCRT complex: A surprise from the Archaea journal March 2009
Orthologs of the small RPB8 subunit of the eukaryotic RNA polymerases are conserved in hyperthermophilic Crenarchaeota and "Korarchaeota" journal January 2007
An Evolutionary Network of Genes Present in the Eukaryote Common Ancestor Polls Genomes on Eukaryotic and Mitochondrial Origin journal January 2012
MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm journal August 2014
Archaeal chromatin and transcription: Chromatin and transcription journal April 2003
MEGAN analysis of metagenomic data journal February 2007
Transcript amplification from single bacterium for transcriptome analysis journal May 2011
Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments journal May 2012
Phylogenetic classification of short environmental DNA fragments journal February 2008
An archaeal origin for the actin cytoskeleton: Implications for eukaryogenesis journal November 2011
The Archaeal Legacy of Eukaryotes: A Phylogenomic Perspective journal July 2014
Binning metagenomic contigs by coverage and composition journal September 2014
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes journal May 2013
An actin-based cytoskeleton in archaea: An archaeal cytoskeleton journal April 2011
Accurate phylogenetic classification of variable-length DNA fragments journal December 2006
Assembling the Marine Metagenome, One Cell at a Time journal April 2009
Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis journal February 2011
The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? journal September 2010
GroopM: an automated tool for the recovery of population genomes from related metagenomes journal January 2014
Insights into the phylogeny and coding potential of microbial dark matter journal July 2013
Phylogenomic Test of the Hypotheses for the Evolutionary Origin of Eukaryotes journal January 2014
Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group journal December 2010
Current opportunities and challenges in microbial metagenome analysis--a bioinformatic perspective journal September 2012
Single cell genomics: an individual look at microbes journal October 2012
Archaebacteria (Archaea) and the origin of the eukaryotic nucleus journal December 2005
Supertrees Disentangle the Chimerical Origin of Eukaryotic Genomes journal May 2007
Eukaryotic evolution, changes and challenges journal March 2006
Archaeal origin of tubulin journal January 2012
Genomic evidence for two functionally distinct gene classes journal May 1998
Archaea in Organic-Lean and Organic-Rich Marine Subsurface Sediments: An Environmental Gradient Reflected in Distinct Phylogenetic Lineages journal January 2012
A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya journal January 2008
A Role for the ESCRT System in Cell Division in Archaea journal December 2008
From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell journal January 2013
A unique cell division machinery in the Archaea journal November 2008
Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge journal November 2010
The PhyloPythiaS Web Server for Taxonomic Assignment of Metagenome Sequences journal June 2012
The Common Ancestor of Archaea and Eukarya Was Not an Archaeon journal January 2013
Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models journal August 2009
From The Cover: Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem journal January 2005
An archaeal origin of eukaryotes supports only two primary domains of life journal December 2013
Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis journal January 2011
The global phylogeny of glycolytic enzymes journal April 2002
The Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of Eukaryotes journal April 2014
Archaeal genetics — the third way journal January 2005
Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage journal May 2013
The origin and early evolution of eukaryotes in the light of phylogenomics journal January 2010
Genomes from Metagenomics journal November 2013
Community structure and metabolism through reconstruction of microbial genomes from the environment journal February 2004
Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. journal August 1996
Genomic Analysis at the Single-Cell Level journal December 2011
Supertrees and symbiosis in eukaryote genome evolution journal October 2007
Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. journal March 1994
Complex archaea that bridge the gap between prokaryotes and eukaryotes journal May 2015
Korarchaeota Diversity, Biogeography, and Abundance in Yellowstone and Great Basin Hot Springs and Ecological Niche Modeling Based on Machine Learning journal May 2012
Microfluidics Expanding the Frontiers of Microbial Ecology journal May 2014
Nucleotide sequence of pig plasma gelsolin journal October 1988
Recent advances in genomic DNA sequencing of microbial species from single cells journal August 2014
Predominant archaea in marine sediments degrade detrital proteins journal March 2013
Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses journal October 2013
Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth journal July 2007
The origins of phagocytosis and eukaryogenesis journal January 2009
Ecology of Sulfur-Oxidizing Bacteria in Hot Acid Soils journal January 1972
Data from: Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes dataset December 2015
Remarkable archaeal diversity detected in a Yellowstone national park hot spring environment journal June 1994
Archaea in Organic-Lean and Organic-Rich Marine Subsurface Sediments: An Environmental Gradient Reflected in Distinct Phylogenetic Lineages text January 2012
Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge text January 2010
Metagenomics: Application of Genomics to Uncultured Microorganisms journal March 2005
Binning Metagenomic Contigs Using Unsupervised Clustering and Reference Databases journal May 2022
Microbiology in transition. journal March 1994
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 journal September 2013
Metagenomics: Application of Genomics to Uncultured Microorganisms journal December 2004
An Overview of Endosymbiotic Models for the Origins of Eukaryotes, Their ATP-Producing Organelles (Mitochondria and Hydrogenosomes), and Their Heterotrophic Lifestyle journal January 2001
Reconstructing each cell's genome within complex microbial communities—dream or reality? journal January 2015
PhyloPythiaS+ : a self-training method for the rapid reconstruction of low-ranking taxonomic bins from metagenomes journal January 2016

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Genotyping of Bartonella bacteria and their animal hosts: current status and perspectives journal August 2017
Asgard archaea illuminate the origin of eukaryotic cellular complexity journal January 2017
Archaea and the origin of eukaryotes journal November 2017
Genomes of two archaeal endosymbionts show convergent adaptations to an intracellular lifestyle journal July 2018
Building de novo reference genome assemblies of complex eukaryotic microorganisms from single nuclei journal January 2020
Energetics and population genetics at the root of eukaryotic cellular and genomic complexity journal December 2015
Integrative modeling of gene and genome evolution roots the archaeal tree of life journal May 2017
Genomic diversity, lifestyles and evolutionary origins of DPANN archaea journal January 2019
Microbial Dark Matter Investigations: How Microbial Studies Transform Biological Knowledge and Empirically Sketch a Logic of Scientific Discovery journal February 2018
Tracing the Archaeal Origins of Eukaryotic Membrane-Trafficking System Building Blocks journal February 2016
Changing ideas about eukaryotic origins journal September 2015
Assessing the viral content of uncultured picoeukaryotes in the global‐ocean by single cell genomics journal September 2019
The Physiology of Phagocytosis in the Context of Mitochondrial Origin 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 journal January 2016
Multiple levels of the unknown in microbiome research journal June 2019
Microbial Community Response to Simulated Petroleum Seepage in Caspian Sea Sediments 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 journal February 2018
Data from: Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes dataset December 2015
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Figures / Tables (7)