On the origin of genomes and cells within inorganic compartments
Open accessAbstract
Building on the model of Russell and Hall for the emergence of life at a warm submarine hydrothermal vent, we suggest that, within a hydrothermally formed system of contiguous iron-sulfide (FeS) compartments, populations of virus-like RNA molecules, which eventually encoded one or a few proteins each, became the agents of both variation and selection. The initial darwinian selection was for molecular self-replication. Combinatorial sorting of genetic elements among compartments would have resulted in preferred proliferation and selection of increasingly complex molecular ensembles--those compartment contents that achieved replication advantages. The last universal common ancestor (LUCA) we propose was not free-living but an inorganically housed assemblage of expressed and replicable genetic elements. The evolution of the enzymatic systems for (i) DNA replication; and (ii) membrane and cell wall biosynthesis, enabled independent escape of the first archaebacterial and eubacterial cells from their hydrothermal hatchery, within which the LUCA itself remained confined.
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Early evolution necessarily involved competition between ensembles of virus-like genetic elements and selection at the level of such collectives.
“This early evolution necessarily involved competition between ensembles of virus-like genetic elements and selection at the level of such collectives (43, 75, 76).”
From Origin and Evolution of the Universal Genetic Code (2017) · cites this paper as [43]
The “Selfish cooperatives” section describes competition among genetic elements and selection of successful compartment-level ensembles. But the paper presents this as a proposed model, not as a necessary feature of all early evolution; the claim’s unqualified “necessarily” overstates it. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe microchambers of alkaline hydrothermal vent systems meet all the basic requirements for a venue for the origin and development of life.
“In short, the microchambers of alkaline hydrothermal vent systems meet all the basic requirements for a venue for the origin and development of life [94,95].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [95]
In “The case for a LUCA confined within a network of inorganic compartments” (page unavailable), the authors argue that warm hydrothermal iron-sulfide compartments could meet the demands of life's emergence by concentrating building blocks, catalyzing reactions, and supplying energy. Our copy does not identify the proposed vents as alkaline, and presents their suitability as a plausible hypothesis rather than an established finding that such systems meet all requirements. (LLM, conf=0.83)
Experimental — accuracy not yet measuredThe deepest, most ancient split in the prokaryotic world is that separating eubacteria from archaebacteria.
“That dichotomy is also mirrored by a number of other cellular, molecular and gene homology attributes, indicating that the deepest, most ancient split in the prokaryotic world is that separating eubacteria from archaebacteria [111,116,122].”
From Early bioenergetic evolution (2013) · cites this paper as [116]
All the developments up to this point took place in a vent microchamber complex.
“We think all the developments up to this point took place in a vent microchamber complex [95].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [95]
Early pre-cellular evolution involved competition between ensembles of virus-like genetic elements and selection at the level of such collectives.
“This early evolution is thought to have involved competition between ensembles of “virus-like” genetic elements and selection at the level of such collectives [30,31,32].”
From Frozen Accident Pushing 50: Stereochemistry, Expansion, and Chance in the Evolution of the Genetic Code (2017) · cites this paper as [32]
Cellularization, in the sense of being encapsulated in such a way that enabled full autonomy, evolved after LUCA.
“Taken at face value, these data suggest that cellularization, in the sense of being encapsulated in such a way that enabled full autonomy, evolved after LUCA [50,64] (Table 1, criterion 5).”
From ‘Whole Organism’, Systems Biology, and Top-Down Criteria for Evaluating Scenarios for the Origin of Life (2021) · cites this paper as [50]
Full cellular autonomy and motility occurred post-LUCA.
“Top-down data also indicate that a complex metabolism predated ribozymes and enzymes, and that full cellular autonomy and motility occurred post-LUCA.”
From ‘Whole Organism’, Systems Biology, and Top-Down Criteria for Evaluating Scenarios for the Origin of Life (2021) · cites this paper as [50]
Under the microchamber complex scenario, the divergence of Bacteria and Archaea occurred within the ancestral microchamber complex.
“Under the microchamber complex scenario this divergence occurred within the ancestral microchamber complex [50,64].”
From ‘Whole Organism’, Systems Biology, and Top-Down Criteria for Evaluating Scenarios for the Origin of Life (2021) · cites this paper as [50]
Archaea and Bacteria use unrelated pathways to synthesize chemically distinct membrane phospholipids.
“Archaea and Bacteria use unrelated pathways to synthesize chemically distinct membrane phospholipids; therefore, it has been proposed that LUCA did not use phospholipids in its membrane, and may have used mineral structure as a means of compartmentation or been totally acellular (Koonin and Martin 2005;Koga et al. 1998).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Koonin and Martin 2005
It has been proposed that LUCA did not use phospholipids in its membrane and may have used mineral structure for compartmentation or been totally acellular.
“Archaea and Bacteria use unrelated pathways to synthesize chemically distinct membrane phospholipids; therefore, it has been proposed that LUCA did not use phospholipids in its membrane, and may have used mineral structure as a means of compartmentation or been totally acellular (Koonin and Martin 2005;Koga et al. 1998).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Koonin and Martin 2005
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Comparative and functional genomics of closteroviruses
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The early evolution of lipid membranes and the three domains of life
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Fungal Diversity in Deep-Sea Hydrothermal Ecosystems
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“by a number of other cellular, molecular and gene homology attributes, indicating that the deepest, most ancient split in the prokaryotic world is that separating eubacteria from archaebacteria [111,116,122].”
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The Drive to Life on Wet and Icy Worlds
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“Strung together on a peptide-like backbone, these RNAs could act as the first transportable genes (Koonin and Martin, 2005; Goodwin et al., 2012).”
InfluentialComparative genomic analyses of nickel, cobalt and vitamin B12 utilization
Zhang, Y., Rodionov, D. A., Gelfand, M. S., & Gladyshev, V. N. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-78 · Cited by 286 · see citing works
Multiple origins of viral capsid proteins from cellular ancestors
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Self-citationThe Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups
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Self-citationFrom volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya
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Emerging critical roles of Fe–S clusters in DNA replication and repair
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Darwinian evolution in the light of genomics
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Self-citationWolf, Y. I., & Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-14 · Cited by 235 · see citing works
“The models detailed in the next section depend on the existence of a certain level of complexity in the RNA world – manifested not only in the diversity of catalytic activities but also in the existence of co-selected ensembles of replicating RNA molecules, the "selfish cooperators" [74].”
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Koonin, E. V., & Dolja, V. V. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00049-13 · Cited by 242 · see citing works
Self-citationViruses take center stage in cellular evolution.
Claverie, J. (2006) · Genome biology · doi:10.1186/gb-2006-7-6-110 · Cited by 237 · see citing works
Nitrifier genomics and evolution of the nitrogen cycle
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Bio-inspired CO 2 conversion by iron sulfide catalysts under sustainable conditions
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Rooting the tree of life by transition analyses.
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Origin of viruses: primordial replicators recruiting capsids from hosts
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Self-citationThe Major Transitions in Evolution Revisited
(2011) · The MIT Press eBooks · doi:10.7551/mitpress/9780262015240.001.0001 · Cited by 220 · see citing works
Origin and Evolution of the Universal Genetic Code
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Self-citationEvolutionary genomics of archaeal viruses: Unique viral genomes in the third domain of life
Prangishvili, D. A., Garrett, R. A., & Koonin, E. V. (2006) · Virus Research · doi:10.1016/j.virusres.2006.01.007 · Cited by 218 · see citing works
Self-citationThe Origin and Nature of Life on Earth: The Emergence of the Fourth Geosphere
Smith, E., & Morowitz, H. J. (2016) · doi:10.1017/cbo9781316348772 · Cited by 215 · see citing works
Once upon a time the cell membranes: 175 years of cell boundary research
Lombard, J. (2014) · Biology Direct · doi:10.1186/s13062-014-0032-7 · Cited by 211 · see citing works
Serpentinite and the dawn of life
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Inventing the dynamo machine: the evolution of the F-type and V-type ATPases
Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., & Koonin, E. V. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1767 · Cited by 210 · see citing works
Self-citationArchaea — timeline of the third domain
Cavicchioli, R. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2482 · Cited by 201 · see citing works
An origin-of-life reactor to simulate alkaline hydrothermal vents
Herschy, B., Whicher, A., Camprubi, E., Watson, C., Dartnell, L., Ward, J., Evans, J. R. G., & Lane, N. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9658-4 · Cited by 194 · see citing works
The last universal common ancestor between ancient Earth chemistry and the onset of genetics
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Self-citationOn the universal core of bioenergetics
Schoepp‐Cothenet, B., van Lis, R., Atteia, A., Baymann, F., Capowiez, L., Ducluzeau, A., Duval, S., ten Brink, F., Russell, M. J., & Nitschke, W. (2012) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2012.09.005 · Cited by 184 · see citing works
The inevitable journey to being
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The Emergence and Early Evolution of Biological Carbon-Fixation
Braakman, R., & Smith, E. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002455 · Cited by 173 · see citing works
Evolution of microbes and viruses: a paradigm shift in evolutionary biology?
Koonin, E. V., & Wolf, Y. I. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00119 · Cited by 171 · see citing works
Self-citationCo-evolution of primordial membranes and membrane proteins
Mulkidjanian, A. Y., Galperin, M. Y., & Koonin, E. V. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.01.005 · Cited by 169 · see citing works
Self-citationTransient compartmentalization of RNA replicators prevents extinction due to parasites
Matsumura, S., Kun, Á., Ryckelynck, M., Coldren, F., Szilágyi, A., Jossinet, F., Rick, C., Nghe, P., Szathmáry, E., & Griffiths, A. D. (2016) · Science · doi:10.1126/science.aag1582 · Cited by 162 · see citing works
Viruses and mobile elements as drivers of evolutionary transitions
Koonin, E. V. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0442 · Cited by 161 · see citing works
Self-citationSpitzer, J. J., & Poolman, B. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00010-09 · Cited by 152 · see citing works
The Evolution of Antiviral Defense Systems
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Isoprenoid biosynthesis in Archaea – Biochemical and evolutionary implications
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Beating the acetyl coenzyme A-pathway to the origin of life
Nitschke, W., & Russell, M. J. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0258 · Cited by 143 · see citing works
Physical foundations of biological complexity
Wolf, Y. I., Katsnelson, M. I., & Koonin, E. V. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807890115 · Cited by 151 · see citing works
Self-citationDid life originate from a global chemical reactor?
Stüeken, E. E., Anderson, R. E., Bowman, J. S., Brazelton, W. J., Colangelo-Lillis, J. R., Goldman, A. D., Som, S. M., & Baross, J. A. (2013) · Geobiology · doi:10.1111/gbi.12025 · Cited by 130 · see citing works
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Mulkidjanian, A. Y., & Galperin, M. Y. (2009) · Biology Direct · doi:10.1186/1745-6150-4-27 · Cited by 130 · see citing works
The Alkaline Solution to the Emergence of Life: Energy, Entropy and Early Evolution
Russell, M. J. (2007) · Acta Biotheoretica · doi:10.1007/s10441-007-9018-5 · Cited by 126 · see citing works
On the Origin of Cells and Viruses
Koonin, E. V. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04992.x · Cited by 122 · see citing works
Self-citationHorizontal Gene Transfer and the History of LifePreprint
Daubin, V., & Szöllősi, G. J. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018036 · Cited by 122 · see citing works
Yamaguchi, A., Yamamoto, M., Takai, K., Ishii, T., Hashimoto, K., & Nakamura, R. (2014) · Electrochimica Acta · doi:10.1016/j.electacta.2014.07.078 · Cited by 119 · see citing works
Origin and evolution of metabolic pathways
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Mulkidjanian, A. Y. (2009) · Biology Direct · doi:10.1186/1745-6150-4-26 · Cited by 117 · see citing works
Becerra, A., Delaye, L., Islas, S., & Lazcano, A. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.38.091206.095825 · Cited by 115 · see citing works
The Biological Big Bang model for the major transitions in evolution
Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-21 · Cited by 115 · see citing works
Self-citationCompositional complementarity and prebiotic ecology in the origin of life
Hunding, A., Képès, F., Lancet, D., Minsky, A., Norris, V., Raine, D. J., Sriram, K., & Root-Bernstein, R. S. (2006) · BioEssays · doi:10.1002/bies.20389 · Cited by 110 · see citing works
Electrical Current Generation across a Black Smoker Chimney
Nakamura, R., Takashima, T., Kato, S., Takai, K., Yamamoto, M., & Hashimoto, K. (2010) · Angewandte Chemie International Edition · doi:10.1002/anie.201003311 · Cited by 111 · see citing works
Towards a processual microbial ontology
Bapteste, E. P., & Dupré, J. (2012) · Biology & Philosophy · doi:10.1007/s10539-012-9350-2 · Cited by 112 · see citing works
The LUCA and its complex virome
Krupovìč, M., Dolja, V. V., & Koonin, E. V. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0408-x · Cited by 110 · see citing works
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Cooperation for direct fitness benefits
Leimar, O., & Hammerstein, P. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0116 · Cited by 112 · see citing works
Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane
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Turnstiles and bifurcators: The disequilibrium converting engines that put metabolism on the road
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Takeuchi, N., & Hogeweg, P. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000542 · Cited by 104 · see citing works
Klotz, M. G. (2010) · Frontiers in Microbiology · doi:10.3389/fmicb.2010.00001 · Cited by 102 · see citing works
Getting a better picture of microbial evolution en route to a network of genomes
Dagan, T., & Martin, W. F. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0040 · Cited by 101 · see citing works
Self-citationIron-Sulfide-Bearing Chimneys as Potential Catalytic Energy Traps at Life's Emergence
Mielke, R. E., Robinson, K. J., White, L. M., McGlynn, S. E., McEachern, K., Bhartia, R., Kanik, I., & Russell, M. J. (2011) · Astrobiology · doi:10.1089/ast.2011.0667 · Cited by 95 · see citing works
The Quest for a Universal Theory of Life
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893 · Cited by 122 · see citing works
Inevitability of Genetic Parasites
Iranzo, J., Puigbò, P., Lobkovsky, A. E., Wolf, Y. I., & Koonin, E. V. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw193 · Cited by 90 · see citing works
Self-citationGenome Networks Root the Tree of Life between Prokaryotic Domains
Dagan, T., Roettger, M., Bryant, D., & Martin, W. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq025 · Cited by 87 · see citing works
Self-citationArchaeology of Eukaryotic DNA Replication
Makarova, K. S., & Koonin, E. V. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012963 · Cited by 87 · see citing works
Self-citationKoonin, E. (2017) · Life · doi:10.3390/life7020022 · Cited by 85 · see citing works
“like” genetic elements and selection at the level of such collectives [30-32].”
BackgroundSelf-citationAncient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics
Dibrova, D. V., Galperin, M. Y., Koonin, E. V., & Mulkidjanian, A. Y. (2015) · Biochemistry (Moscow) · doi:10.1134/s0006297915050016 · Cited by 78 · see citing works
Self-citationPumice as a Remarkable Substrate for the Origin of Life
Brasier, M. D., Matthewman, R., McMahon, S., & Wacey, D. (2011) · Astrobiology · doi:10.1089/ast.2010.0546 · Cited by 86 · see citing works
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The fundamental units, processes and patterns of evolution, and the Tree of Life conundrum
Koonin, E. V., & Wolf, Y. I. (2009) · Biology Direct · doi:10.1186/1745-6150-4-33 · Cited by 74 · see citing works
Self-citationViruses and cells intertwined since the dawn of evolution
Durzyńska, J., & Goździcka‐Józefiak, A. (2015) · Virology Journal · doi:10.1186/s12985-015-0400-7 · Cited by 75 · see citing works
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Takeuchi, N., Hogeweg, P., & Koonin, E. V. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002024 · Cited by 69 · see citing works
Self-citationA general model on the origin of biological codes
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Evolution of complexity in RNA-like replicator systems
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Early evolution without a tree of life
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Self-citationThe lipid bilayer membrane and its protein constituents
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The Nature of Life: Classical and Contemporary Perspectives from Philosophy and Science
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Origins of Life: The Primal Self-Organization
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Structural Co-Evolution of Viruses and Cells in the Primordial World
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The Origin of Life: Chemical Evolution of a Metabolic System in a Mineral Honeycomb?
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Gene content of LUCA, the last universal common ancestor
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- Authors
- Koonin, E. V., & Martin, W.
- Affiliations
- National Institutes of Health (US)
- Heinrich Heine University Düsseldorf (DE)
- Corresponding author
- Koonin, Eugene V.
- Venue
- Trends in Genetics
- Publisher
- Elsevier BV
- Published
- 2005-12
- Volume
- 21
- Issue
- 12
- Pages
- 647-654
- ISSN
- 0168-9525 (ISSN-L)
- PMC
- PMC7172762
- OpenAlex
- W2141847401
- Cited by
- 406
- References
- 87
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 21 · 2023: 14 · 2022: 10 · 2021: 20 · 2020: 17 · 2019: 42 · 2018: 20 · 2017: 15 · 2016: 16 · 2015: 14 · 2014: 18 · 2013: 17 · 2012: 25
- FWCI
- 2.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Trends in Genetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- origin of life, hydrothermal vents, Darwinian selection, last universal common ancestor, compartmentalization, membrane biosynthesis, cell wall biosynthesis, archaea, eubacteria, origin of cells
- MeSH terms
- Origin of Life, DNA, RNA, Genome, Bacterial, Evolution, Molecular, Genome, Archaeal
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