Archaeal Histone Contributions to the Origin of Eukaryotes
Open accessAbstract
The eukaryotic lineage arose from bacterial and archaeal cells that underwent a symbiotic merger. At the origin of the eukaryote lineage, the bacterial partner contributed genes, metabolic energy, and the building blocks of the endomembrane system. What did the archaeal partner donate that made the eukaryotic experiment a success? The archaeal partner provided the potential for complex information processing. Archaeal histones were crucial in that regard by providing the basic functional unit with which eukaryotes organize DNA into nucleosomes, exert epigenetic control of gene expression, transcribe genes with CCAAT-box promoters, and a manifest cell cycle with condensed chromosomes. While mitochondrial energy lifted energetic constraints on eukaryotic protein production, histone-based chromatin organization paved the path to eukaryotic genome complexity, a critical hurdle en route to the evolution of complex cells.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The origin of the modern eukaryotic cell was dependent on the origin of histone-like proteins in the archaeal partner and oxidative phosphorylation in the bacterial partner.
“The origin of the modern eukaryotic cell was dependent on the origin of histone-like proteins in the archaeal partner [19], and oxidative phosphorylation in the bacterial partner [20,21]”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [19]
The genetic core in the emerging nucleus became organized into chromosomes built around histone proteins provided by the archaeon and contains a mixture of genes from the archaeal partner and genes transferred from the developing mitochondria.
“The genetic core in the emerging nucleus became organized into chromosomes built around histone proteins provided by archaeon [19] and contains a mixture of genes from the archaeal partner and genes transferred from the developing mitochondria (bacterial partner) [21,161,162].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [19]
Eukaryotic DNA is organized into linear chromosomes composed of chromatin facilitated by histones, DNA binding proteins that form regular compact structures.
“Eukaryotic DNA is organized into linear chromosomes composed of chromatin facilitated by histones, DNA binding proteins that form regular compact structures [19].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [19]
Cites
Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · see citing works
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679 · see citing works
The AMPK signalling pathway coordinates cell growth, autophagy and metabolism
Mihaylova, M. M., & Shaw, R. J. (2011) · Nature Cell Biology · doi:10.1038/ncb2329 · Cited by 2,923 · see citing works
Histone acetylation in chromatin structure and transcription
Grunstein, M. (1997) · Nature · doi:10.1038/38664 · Cited by 2,884 · see citing works
Selfish DNA: the ultimate parasite
Orgel, L. E., & Crick, F. H. C. (1980) · Nature · doi:10.1038/284604a0 · Cited by 2,163 · see citing works
Jung, C. H., Ro, S.-H., Cao, J., Otto, N. M., & Kim, D.-H. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.01.017 · Cited by 2,090 · see citing works
On the origin of mitosing cells
Sagan, L. (1967) · Journal of Theoretical Biology · doi:10.1016/0022-5193(67)90079-3 · Cited by 1,870 · see citing works
Dent, S., Denu, J. M., & Allis, C. D. (2001) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.70.1.81 · Cited by 1,844 · see citing works
Fox, G. E., Stackebrandt, E. S., Hespell, R. B., Gibson, J., Maniloff, J., Dyer, T. A., Wolfe, R. S., Balch, W. E., Tanner, R. S., Magrum, L. J., et al. (1980) · Science · doi:10.1126/science.6771870 · Cited by 1,458 · see citing works
Complex archaea that bridge the gap between prokaryotes and eukaryotes
Spang, A., Saw, J. H., Jørgensen, S. L., Zaremba-Niedzwiedzka, K., Martijn, J., Lind, A. E., van Eijk, R., Schleper, C., Guy, L., & Ettema, T. J. G. (2015) · Nature · doi:10.1038/nature14447 · Cited by 1,324 · see citing works
The energetics of genome complexity.
Lane, N., & Martin, W. (2010) · Nature · doi:10.1038/nature09486 · Cited by 1,289 · see citing works
Self-citationThe Hydrogen Hypothesis for the First Eukaryote
Martin, W., & Müller, M. (1998) · Nature · doi:10.1038/32096 · Cited by 1,282 · see citing works
Self-citationAsgard archaea illuminate the origin of eukaryotic cellular complexity
Zaremba-Niedzwiedzka, K., Caceres, E. F., Saw, J. H., Bäckström, D., Juzokaite, L., Vancaester, E., Seitz, K. W., Anantharaman, K., Starnawski, P., Kjeldsen, K. U., et al. (2017) · Nature · doi:10.1038/nature21031 · Cited by 1,226 · see citing works
Bücher, P. (1990) · Journal of Molecular Biology · doi:10.1016/0022-2836(90)90223-9 · Cited by 1,118 · see citing works
Histone acetylation: a switch between repressive and permissive chromatin
Eberharter, A., & Becker, P. B. (2002) · EMBO Reports · doi:10.1093/embo-reports/kvf053 · Cited by 944 · see citing works
ChromEMT: Visualizing 3D chromatin structure and compaction in interphase and mitotic cells
Ou, H. D., Phan, S., Deerinck, T. J., Thor, A., Ellisman, M. H., & O’Shea, C. C. (2017) · Science · doi:10.1126/science.aag0025 · Cited by 872 · see citing works
The molecular biology of the CCAAT-binding factor NF-Y
Mantovani, R. (1999) · Gene · doi:10.1016/s0378-1119(99)00368-6 · Cited by 861 · see citing works
Deatherage, B. L., & Cookson, B. T. (2012) · Infection and Immunity · doi:10.1128/iai.06014-11 · Cited by 765 · see citing works
Woese, C. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132266999 · Cited by 762 · see citing works
New insights into nucleosome and chromatin structure: an ordered state or a disordered affair?
Luger, K., Dechassa, M. L., & Tremethick, D. J. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3382 · Cited by 738 · see citing works
Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process
Woese, C. R., Olsen, G. J., Ibba, M., & Söll, D. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.1.202-236.2000 · Cited by 706 · see citing works
Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma
Gregory, T. R. (2001) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793100005595 · Cited by 699 · see citing works
Histone acetylation and deacetylation in yeast
Kurdistani, S. K., & Grunstein, M. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1075 · Cited by 677 · see citing works
Gould, S. B., Waller, R. F., & McFadden, G. I. (2008) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.59.032607.092915 · Cited by 634 · see citing works
Content of carbon, nitrogen, oxygen, sulfur and phosphorus in native aquatic and cultured bacteria
Fagerbakke, K., Heldal, M., & Norland, S. (1996) · Aquatic Microbial Ecology · doi:10.3354/ame010015 · Cited by 609 · see citing works
Endosymbiotic theories for eukaryote origin
Martin, W. F., Garg, S., & Zimorski, V. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0330 · Cited by 583 · see citing works
Self-citationThe ring of life provides evidence for a genome fusion origin of eukaryotes
Rivera, M. C., & Lake, J. A. (2004) · Nature · doi:10.1038/nature02848 · Cited by 546 · see citing works
THE GENETIC ORGANIZATION OF CHROMOSOMES
Thomas, C. A. (1971) · Annual Review of Genetics · doi:10.1146/annurev.ge.05.120171.001321 · Cited by 545 · see citing works
Genomic evidence for two functionally distinct gene classes
Rivera, M. C., Jain, R., Moore, J. E., & Lake, J. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.11.6239 · Cited by 544 · see citing works
An archaeal origin of eukaryotes supports only two primary domains of life
Williams, T. A., Foster, P. G., Cox, C. J., & Embley, T. M. (2013) · Nature · doi:10.1038/nature12779 · Cited by 519 · see citing works
Introns and the origin of nucleus–cytosol compartmentalization
Martin, W. F., & Koonin, E. V. (2006) · Nature · doi:10.1038/nature04531 · Cited by 497 · see citing works
Self-citationTHE DESOXYRIBONUCLEIC ACID CONTENT OF ANIMAL CELLS AND ITS EVOLUTIONARY SIGNIFICANCE
Mirsky, A. E., & Ris, H. (1951) · The Journal of General Physiology · doi:10.1085/jgp.34.4.451 · Cited by 493 · see citing works
Graur, D., Zheng, Y., Price, N. C., Azevedo, R. B. R., Zufall, R. A., & Elhaik, E. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt028 · Cited by 482 · see citing works
Emerging roles of linker histones in regulating chromatin structure and function
Fyodorov, D. V., Zhou, B., Skoultchi, A. I., & Bai, Y. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.94 · Cited by 478 · see citing works
Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin
Betts, H. C., Puttick, M. N., Clark, J. W., Williams, T. A., Donoghue, P. C. J., & Pisani, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0644-x · Cited by 437 · see citing works
Hake, S. B., & Allis, C. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600803103 · Cited by 435 · see citing works
Newly born peroxisomes are a hybrid of mitochondrial and ER-derived pre-peroxisomes
Sugiura, A., Mattie, S., Prudent, J., & McBride, H. M. (2017) · Nature · doi:10.1038/nature21375 · Cited by 386 · see citing works
The vital force; a study of bioenergetics
(1987) · International Journal of Biochemistry · doi:10.1016/0020-711x(87)90076-0 · Cited by 369 · see citing works
Endosymbiotic origin and differential loss of eukaryotic genes
Ku, C., Sathi, S. N., Roettger, M., Sousa, F. L., Lockhart, P. J., Bryant, D., Hazkani‐Covo, E., McInerney, J. O., Landan, G., & Martin, W. F. (2015) · Nature · doi:10.1038/nature14963 · Cited by 346 · see citing works
Self-citationHigher-Order Structures of Chromatin: The Elusive 30 nm Fiber
Tremethick, D. J. (2007) · Cell · doi:10.1016/j.cell.2007.02.008 · Cited by 344 · see citing works
Metabolic Regulation of Histone Post-Translational Modifications
Fan, J., Krautkramer, K. A., Feldman, J. L., & Denu, J. M. (2015) · ACS Chemical Biology · doi:10.1021/cb500846u · Cited by 334 · see citing works
Esser, C. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh160 · Cited by 324 · see citing works
What's in a genome? The C-value enigma and the evolution of eukaryotic genome content
Elliott, T. A., & Gregory, T. R. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0331 · Cited by 323 · see citing works
Nutrient-Sensing Mechanisms across Evolution
Chantranupong, L., Wolfson, R. L., & Sabatini, D. M. (2015) · Cell · doi:10.1016/j.cell.2015.02.041 · Cited by 320 · see citing works
Romier, C., Cocchiarella, F., Mantovani, R., & Moras, D. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209635200 · Cited by 306 · see citing works
Extreme Bendability of DNA Less than 100 Base Pairs Long Revealed by Single-Molecule Cyclization
Vafabakhsh, R., & Ha, T. (2012) · Science · doi:10.1126/science.1224139 · Cited by 301 · see citing works
Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes.
Lake, J. A., Henderson, E. R., Oakes, M., & Clark, M. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.12.3786 · Cited by 296 · see citing works
Emerging roles for chromatin as a signal integration and storage platform
Badeaux, A. I., & Shi, Y. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3545 · Cited by 291 · see citing works
DNA Replication in the Archaea
Barry, E. R., & Bell, S. D. (2006) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00029-06 · Cited by 286 · see citing works
Transposable genetic elements as agents of gene instability and chromosomal rearrangements
Nevers, P., & Saedler, H. (1977) · Nature · doi:10.1038/268109a0 · Cited by 274 · see citing works
Epigenetic mechanisms elicited by nutrition in early life
Canani, R. B., Costanzo, M. D., Leone, L., Bedogni, G., Brambilla, P., Cianfarani, S., Nobili, V., Pietrobelli, A., & Agostoni, C. V. (2011) · Nutrition Research Reviews · doi:10.1017/s0954422411000102 · Cited by 229 · see citing works
Sandman, K., Krzycki, J. A., Dobrinski, B., Lurz, R., & Reeve, J. N. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.15.5788 · Cited by 215 · see citing works
The Bacterial Actin-Like Cytoskeleton
Carballido‐López, R. (2006) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00014-06 · Cited by 214 · see citing works
Autophagy: The Last Defense against Cellular Nutritional Stress
He, L., Zhang, J., Zhao, J., Ma, N., Kim, S. W., Qiao, S., & Ma, X. (2018) · Advances in Nutrition · doi:10.1093/advances/nmy011 · Cited by 209 · see citing works
Cunha, V. D., Gaïa, M., Gadelle, D., Nasir, A., & Forterre, P. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006810 · Cited by 206 · see citing works
Structure of histone-based chromatin in Archaea
Mattiroli, F., Bhattacharyya, S., Dyer, P. N., White, A. E., Sandman, K., Burkhart, B. W., Byrne, K. R., Lee, T., Ahn, N. G., Santangelo, T. J., et al. (2017) · Science · doi:10.1126/science.aaj1849 · Cited by 206 · see citing works
Nutrient control of TORC1, a cell-cycle regulator
Wang, X., & Proud, C. G. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.03.005 · Cited by 197 · see citing works
Bacterial Vesicle Secretion and the Evolutionary Origin of the Eukaryotic Endomembrane System
Gould, S. B., Garg, S. G., & Martin, W. F. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.03.005 · Cited by 193 · see citing works
Self-citationSupertrees Disentangle the Chimerical Origin of Eukaryotic Genomes
Pisani, D., Cotton, J. A., & McInerney, J. O. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm095 · Cited by 187 · see citing works
Functional coupling between writers, erasers and readers of histone and DNA methylation
Torres, I. O., & Fujimori, D. G. (2015) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2015.09.007 · Cited by 179 · see citing works
Skeletal DNA and the Evolution of Genome Size
Cavalier‐Smith, T. (1982) · Annual Review of Biophysics and Bioengineering · doi:10.1146/annurev.bb.11.060182.001421 · Cited by 173 · see citing works
Greater Than the Sum of Parts: Complexity of the Dynamic Epigenome
Soshnev, A. A., Josefowicz, S. Z., & Allis, C. D. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.05.004 · Cited by 172 · see citing works
How the cell cycle impacts chromatin architecture and influences cell fate
Ma, Y., Kanakousaki, K., & Buttitta, L. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00019 · Cited by 158 · see citing works
Dynamic Recruitment of NF-Y and Histone Acetyltransferases on Cell-cycle Promoters
Caretti, G., Salsi, V., Vecchi, C., Imbriano, C., & Mantovani, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304606200 · Cited by 153 · see citing works
The Physiology of Phagocytosis in the Context of Mitochondrial Origin
Martin, W. F., Tielens, A. G. M., Mentel, M., Garg, S. G., & Gould, S. B. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00008-17 · Cited by 152 · see citing works
Self-citationErickson, H. (2007) · BioEssays · doi:10.1002/bies.20601 · Cited by 151 · see citing works
Theory of DNA condensation: Collapse versus aggregation
Post, C. B., & Zimm, B. H. (1982) · Biopolymers · doi:10.1002/bip.360211104 · Cited by 146 · see citing works
The hybrid nature of the Eukaryota and a consilient view of life on Earth
McInerney, J. O., O’Connell, M. J., & Pisani, D. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3271 · Cited by 138 · see citing works
Evolution of cytomotive filaments: The cytoskeleton from prokaryotes to eukaryotes
Löwe, J., & Amos, L. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.08.010 · Cited by 135 · see citing works
Archaeal histones and the origin of the histone fold
Sandman, K., & Reeve, J. N. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.08.003 · Cited by 128 · see citing works
Cavalier‐Smith, T. (1989) · Nature · doi:10.1038/339100a0 · Cited by 119 · see citing works
The energy expansions of evolution
Judson, O. P. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0138 · Cited by 118 · see citing works
Eukaryogenesis, how special really?
Booth, A., & Doolittle, W. F. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421376112 · Cited by 116 · see citing works
Diversity of prokaryotic chromosomal proteins and the origin of the nucleosome
Sandman, K., Pereira, S. L., & Reeve, J. N. (1998) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050259 · Cited by 116 · see citing works
Structure and function of archaeal histones
Henneman, B., van Emmerik, C. L., van Ingen, H., & Dame, R. T. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007582 · Cited by 111 · see citing works
Histone-Modifying Enzymes: Regulators of Developmental Decisions and Drivers of Human Disease
Napierala, J. S., Koutelou, E., Schibler, A. C., & Dent, S. (2012) · Epigenomics · doi:10.2217/epi.12.3 · Cited by 107 · see citing works
Gould, S. B. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.086 · Cited by 101 · see citing works
Histone-like protein in the prokaryote Thermoplasma acidophilum
Searcy, D. G. (1975) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(75)90076-3 · Cited by 94 · see citing works
Cotton, J. A., & McInerney, J. O. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000265107 · Cited by 91 · see citing works
Peng, Y., & Jahroudi, N. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m213156200 · Cited by 90 · see citing works
The Archaebacteria and eukaryotic origins
Valen, L. M. V., & Maiorana, V. C. (1980) · Nature · doi:10.1038/287248a0 · Cited by 87 · see citing works
Gene-based predictive models of trophic modes suggest Asgard archaea are not phagocytotic
Burns, J. A., Pittis, A. A., & Kim, E. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0477-7 · Cited by 82 · see citing works
Archaebacteria and the Origin of the Eukaryotic Cytoplasm
Zillig, W., Schnabel, R., & STETTER, K. O. (1985) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-70227-3_1 · Cited by 79 · see citing works
On the Archaeal Origins of Eukaryotes and the Challenges of Inferring Phenotype from Genotype
Dey, G., Thattai, M., & Baum, B. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.03.009 · Cited by 78 · see citing works
Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor
Garg, S. G., & Martin, W. F. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw136 · Cited by 76 · see citing works
Self-citationČuboňová, L., Sandman, K., Hallam, S., DeLong, E. F., & Reeve, J. N. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.15.5482-5485.2005 · Cited by 70 · see citing works
Serial endosymbiosis or singular event at the origin of eukaryotes?
Lane, N. J. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.04.031 · Cited by 69 · see citing works
Reciprocal Regulation of AMPK/SNF1 and Protein Acetylation
Vančura, A., Nagar, S., Kaur, P., Bu, P., Bhagwat, M., & Vancurova, I. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113314 · Cited by 67 · see citing works
Evidence for a protein domain superfamily shared by the cyclins, TFIIB and RB/p107
Gibson, T. J., Thompson, J., Blocker, A., & Kouzarides, T. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.6.946 · Cited by 66 · see citing works
DNA Minor Groove Sensing and Widening by the CCAAT-Binding Complex
Huber, E. M., Scharf, D. H., Hortschansky, P., Groll, M., & Brakhage, A. A. (2012) · Structure · doi:10.1016/j.str.2012.07.012 · Cited by 62 · see citing works
Histone H3 N-terminus regulates higher order structure of yeast heterochromatin
Sperling, A. S., & GRUNSTEIN, M. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906866106 · Cited by 60 · see citing works
Reactive Acyl-CoA Species Modify Proteins and Induce Carbon Stress
Trub, A. G., & Hirschey, M. D. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.02.002 · Cited by 59 · see citing works
Was the Mitochondrion Necessary to Start Eukaryogenesis?
Hampl, V., Čepička, I., & Eliáš, M. (2018) · Trends in Microbiology · doi:10.1016/j.tim.2018.10.005 · Cited by 57 · see citing works
Peeters, J. G. C., Picavet, L. W., Coenen, S. G. J. M., Mauthe, M., Vervoort, S. J., Mocholi, E., de Heus, C., Klumperman, J., Vastert, S. J., Reggiori, F., et al. (2019) · Autophagy · doi:10.1080/15548627.2018.1509608 · Cited by 55 · see citing works
A MYCOPLASMA-LIKE ARCHAEBACTERIUM POSSIBLY RELATED TO THE NUCLEUS AND CYTOPLASM OF EUKARYOTIC CELLS
Searcy, D. G., Stein, D. B., & Searcy, K. B. (1981) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1981.tb54373.x · Cited by 53 · see citing works
Steps on the road to eukaryotes
Embley, T. M., & Williams, T. A. (2015) · Nature · doi:10.1038/nature14522 · Cited by 42 · see citing works
Nucleosomes: a Solution to a Crowded Intracellular Environment?
Minsky, A., Ghirlando, R., & Reich, Z. (1997) · Journal of Theoretical Biology · doi:10.1006/jtbi.1997.0525 · Cited by 42 · see citing works
A MYCOPLASMA-LIKE ARCHAEBACTERIUM POSSIBLY RELATED TO THE NUCLEUS AND CYTOPLASM OF EUKARYOTIC CELLS
Searcy, D. G., Stein, D. B., & Searcy, K. B. (1981) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1981.tb46527.x · Cited by 41 · see citing works
Symbiogenesis, gradualism, and mitochondrial energy in eukaryote origin
Martin, W. F. (2017) · Periodicum Biologorum · doi:10.18054/pb.v119i3.5694 · Cited by 38 · see citing works
Self-citationMitochondria are not captive bacteria
Harish, A., & Kurland, C. G. (2017) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2017.07.011 · Cited by 34 · see citing works
Beckwith, S. L., Schwartz, E. K., García-Nieto, P. E., King, D. A., Gowans, G. J., Wong, K. M., Yao, W., Eckley, T. L., Paraschuk, A. P., Peltan, E. L., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007216 · Cited by 34 · see citing works
Are There Rab GTPases in Archaea?
Surkont, J., & Pereira‐Leal, J. B. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw061 · Cited by 29 · see citing works
Hara, F., Yamashiro, K., Nemoto, N., Ohta, Y., Yokobori, S.-I., Yasunaga, T., Hisanaga, S.-I., & Yamagishi, A. (2007) · Journal of Bacteriology · doi:10.1128/jb.01454-06 · Cited by 29 · see citing works
An Evolutionary Framework for Understanding the Origin of Eukaryotes
Blackstone, N. W. (2016) · Biology · doi:10.3390/biology5020018 · Cited by 27 · see citing works
Diversity of the DNA Replication System in the Archaea Domain
Sarmiento, F., Long, F., Cann, I., & Whitman, W. B. (2014) · Archaea · doi:10.1155/2014/675946 · Cited by 24 · see citing works
Origin of the Eukaryotic Nucleus
Sandman, K., & Reeve, J. N. (1998) · Science · doi:10.1126/science.280.5363.499d · Cited by 19 · see citing works
The vital force: A study of bioenergetics
(1987) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(87)90121-2 · Cited by 14 · see citing works
Mitochondria and endomembrane origins
McBride, H. M. (2018) · Current Biology · doi:10.1016/j.cub.2018.03.052 · Cited by 13 · see citing works
Mind the gaps in cellular evolution
McInerney, J. O., & O’Connell, M. J. (2017) · Nature · doi:10.1038/nature21113 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Isolation of an archaeon at the prokaryote–eukaryote interface
Imachi, H., Nobu, M. K., Nakahara, N., Morono, Y., Ogawara, M., Takaki, Y., Takano, Y., Uematsu, K., Ikuta, T., Ito, M., et al. (2020) · Nature · doi:10.1038/s41586-019-1916-6 · Cited by 624 · see citing works
Isolation of an archaeon at the prokaryote-eukaryote interfacePreprint
Imachi, H., Nobu, M. K., Nakahara, N., Morono, Y., Ogawara, M., Takaki, Y., Takano, Y., Uematsu, K., Ikuta, T., Ito, M., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/726976 · Cited by 150 · see citing works
Phenomenal Consciousness and Emergence: Eliminating the Explanatory Gap
Feinberg, T. E., & Mallatt, J. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01041 · Cited by 78 · see citing works
“For accounts of this evolutionary sequence of emergent features, see Lane and Martin (2010), Feinberg and Mallatt (2016a), Brunet et al. (2019), Brunk and Martin (2019), and Watson (2019).”
BackgroundTCA cycle signalling and the evolution of eukaryotes
Ryan, D. G., Frezza, C., & O'Neill, L. A. J. (2020) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2020.09.014 · Cited by 69 · see citing works
Histone variants in archaea and the evolution of combinatorial chromatin complexity
Stevens, K. M., Swadling, J. B., Hocher, A., Bang, C., Gribaldo, S., Schmitz, R. A., & Warnecke, T. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2007056117 · Cited by 59 · see citing works
Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
Bowerman, S., Wereszczynski, J., & Luger, K. (2021) · eLife · doi:10.7554/elife.65587 · Cited by 59 · see citing works
Endosymbiotic selective pressure at the origin of eukaryotic cell biology
Raval, P. K., Garg, S. G., & Gould, S. B. (2022) · eLife · doi:10.7554/elife.81033 · Cited by 57 · see citing works
Bacterial Genes Outnumber Archaeal Genes in Eukaryotic Genomes
Brueckner, J., & Martin, W. F. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa047 · Cited by 54 · see citing works
Self-citationNucleosome Positioning and Spacing: From Mechanism to Function
Singh, A. K., & Mueller‐Planitz, F. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.166847 · Cited by 54 · see citing works
Evidence for a Syncytial Origin of Eukaryotes from Ancestral State Reconstruction
Skejo, J., Garg, S. G., Gould, S. B., Hendriksen, M., Tria, F. D. K., Bremer, N., Franjević, D., Blackstone, N. W., & Martin, W. F. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab096 · Cited by 43 · see citing works
Self-citationHäcker, G. A., & Haimovici, A. (2022) · Cell Death and Differentiation · doi:10.1038/s41418-022-01058-0 · Cited by 40 · see citing works
PGC‐1α protects from myocardial ischaemia‐reperfusion injury by regulating mitonuclear communication
Li, Y., Jiao, Y., Liu, Y., Fu, J., Sun, L., & Su, J. (2021) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.16236 · Cited by 38 · see citing works
Irwin, N. A. T., & Richards, T. A. (2024) · Nature Microbiology · doi:10.1038/s41564-024-01707-9 · Cited by 36 · see citing works
An archaeal histone-like protein regulates gene expression in response to salt stress
Sakrikar, S., & Schmid, A. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab1175 · Cited by 31 · see citing works
Shi, W., Zhang, B., Li, M., Liu, K., Jiao, J., & Tian, C. F. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac664 · Cited by 29 · see citing works
Wenck, B. R., & Santangelo, T. J. (2020) · Transcription · doi:10.1080/21541264.2020.1838865 · Cited by 24 · see citing works
Evolution, structure and function of divergent macroH2A1 splice isoforms
Guberović, I., Farkaš, M., Corujo, D., & Buschbeck, M. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.03.036 · Cited by 22 · see citing works
Nucleosomes at the Dawn of Eukaryotes
Hocher, A., & Warnecke, T. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae029 · Cited by 17 · see citing works
Archaeal histone-based chromatin structures regulate transcription elongation rates
Wenck, B. R., Vickerman, R. L., Burkhart, B. W., & Santangelo, T. J. (2024) · Communications Biology · doi:10.1038/s42003-024-05928-w · Cited by 15 · see citing works
Histone Sample Preparation for Bottom-Up Mass Spectrometry: A Roadmap to Informed Decisions
Daled, S., Willems, S., Puyvelde, B. V., Corveleyn, L., Verhelst, S., Clerck, L. D., Deforce, D. L. D., & Dhaenens, M. (2021) · Proteomes · doi:10.3390/proteomes9020017 · Cited by 15 · see citing works
Collens, A. B., & Katz, L. A. (2020) · Journal of Heredity · doi:10.1093/jhered/esaa060 · Cited by 13 · see citing works
Histone clipping: the punctuation in the histone code
Dhaenens, M. (2021) · EMBO Reports · doi:10.15252/embr.202153440 · Cited by 13 · see citing works
Huber, E. M., Hortschansky, P., Scheven, M. T., Misslinger, M., Haas, H., Brakhage, A. A., & Groll, M. (2022) · Structure · doi:10.1016/j.str.2022.04.001 · Cited by 12 · see citing works
Renewing L innaean taxonomy: a proposal to restructure the highest levels of the N atural S ystem
van der Gulik, P. T. S., Hoff, W. D., & Speijer, D. (2022) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12920 · Cited by 11 · see citing works
DNA cytosine methylation suppresses meiotic recombination at the sex-determining region
Ge, T., Gui, X., Xu, J.-X., Xia, W., Wang, C.-H., Yang, W., Huang, K., Walsh, C. P., Umen, J., Walter, J., et al. (2024) · Science Advances · doi:10.1126/sciadv.adr2345 · Cited by 11 · see citing works
Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell
Brunk, C. F., & Marshall, C. R. (2024) · Life · doi:10.3390/life14020226 · Cited by 5 · see citing works
“Eukaryotic DNA is organized into linear chromosomes composed of chromatin facilitated by histones, DNA binding proteins that form regular compact structures [19].”
BackgroundSelf-citationMetagenomic mining reveals novel viral histones in dsDNA viruses
Liu, Y., Hou, Z., Hao, W., Cui, S., Wang, H., & Liu, Y. (2025) · hLife · doi:10.1016/j.hlife.2025.02.005 · Cited by 5 · see citing works
Zheng, F., Yao, W., He, W., Zhang, W., Chen, Y., Chen, H., Zeng, Z., Liu, X., Ding, S., Zheng, Y., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-67286-3 · Cited by 4 · see citing works
An experimental design to extract more information from MS-based histone studies
Clerck, L. D., Willems, S., Daled, S., Puyvelde, B. V., Verhelst, S., Corveleyn, L., Deforce, D. L. D., & Dhaenens, M. (2021) · Molecular Omics · doi:10.1039/d1mo00201e · Cited by 4 · see citing works
Creating a bacterium that forms eukaryotic nucleosome core particles
Jing, X., Zhang, N., Zhou, X., Chen, P., Gong, J., Zhang, K., Wu, X., Cai, W., Ye, B., Hao, P., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-52484-2 · Cited by 3 · see citing works
The contours of evolution: In defence of Darwin's tree of life paradigm
van der Gulik, P. T. S., Hoff, W. D., & Speijer, D. (2024) · BioEssays · doi:10.1002/bies.202400012 · Cited by 3 · see citing works
Povolotsky, T. L., Barazany, H. L., Shacham‐Diamand, Y., & Kolodkin‐Gal, I. (2024) · Biotechnology Advances · doi:10.1016/j.biotechadv.2024.108414 · Cited by 3 · see citing works
Zhou, X., Zhang, N., Gong, J., Zhang, K., Chen, P., Cheng, X. L., Ye, B., Zhao, G., Jing, X., & Li, X. (2024) · Communications Biology · doi:10.1038/s42003-024-07211-4 · Cited by 3 · see citing works
Borchetia, S., Gogoi, M., Rawal, H. C., Patel, P. K., Chakraborty, M., Saikia, H., Nishad, J., R, V. J. I., Barooah, A. K., & Mondal, T. K. (2022) · Journal of Plant Growth Regulation · doi:10.1007/s00344-022-10761-8 · Cited by 3 · see citing works
Self-assembling viral histones unravel early nucleosome evolutionPreprint
Irwin, N. A. T., & Richards, T. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.20.558576 · Cited by 3 · see citing works
Syncytia: From a Historical Resumption to Epigenetic Advances
Casotti, M. C., Zetum, A. S. S., da Silva, D. R. C., Barbosa, D. G., Alvarenga, F. D. S., Giacinti, G. M., Pavan, I. P., Barbosa, K. R. M., Morais, L. C., Altoé, L. S. C., et al. (2025) · DNA and cell biology reports. · doi:10.1089/dcbr.2024.0037 · Cited by 2 · see citing works
Role of mitochondrial outer membrane permeabilization during bacterial infection
Kontchou, C. W., & Häcker, G. A. (2022) · International review of cytology · doi:10.1016/bs.ircmb.2022.10.002 · Cited by 1 · see citing works
The promise of omics approaches for pediatric drug development
Verhelst, S., Goessens, T., Peró-Gascón, R., Boevre, M. D., Impens, F., Deforce, D. L. D., & Dhaenens, M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-88459-4.00011-0 · Cited by 1 · see citing works
Moonlighting Proteins of Human and Some Other Eukaryotes. Evolutionary Aspects
Ss, S. (2025) · Biochemistry (Moscow) · doi:10.1134/s0006297924602855 · Cited by 3 · see citing works
Sakrikar, S., Hackley, R. K., Martínez-Pastor, M., Darnell, C. L., Vreugdenhil, A., & Schmid, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.22.485428 · Cited by 1 · see citing works
Augusto, R. D. C., Minoda, A., Rey, O., Cosseau, C., Chaparro, C., Vidal‐Dupiol, J., Allienne, J., DUVAL, D. T., Pinaud, S., Tönges, S., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/824789
Augusto, R. D. C., Minoda, A., Rey, O., Cosseau, C., Chaparro, C., Vidal‐Dupiol, J., Allienne, J., DUVAL, D. T., Pinaud, S., Tönges, S., et al. (2020) · doi:10.21203/rs.3.rs-31260/v1
Faculty Opinions recommendation of Isolation of an archaeon at the prokaryote-eukaryote interface.
Nester, G. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737211418.793572208
Faculty Opinions recommendation of Isolation of an archaeon at the prokaryote-eukaryote interface.
Galperin, M. Y. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737211418.793572907
Raval, P. K., Zimorski, V., & Martin, W. F. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15750-9.00011-2
Self-citationEpigenetics in personalized toxicity
Corveleyn, L., Verhelst, S., Deforce, D. L. D., & Dhaenens, M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23802-4.00022-3
General Characteristics and Properties of Organic Life
Knoflacher, M. (2024) · Springer eBooks · doi:10.1007/978-3-662-69423-7_5
Bulgheresi, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-18789-6.00009-0
Bulgheresi, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-18789-6.00006-5
ArchLips: A comprehensive in silico database for high-throughput identification of archaeal lipidsPreprint
Zheng, F., Yao, W., He, W., Zhang, W., Chen, Y., Chen, H., Zeng, Z., Liu, X., Ding, S., Zheng, Y., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.05.652033
Vandemoortele, B., Corveleyn, L., Vanhooren, J., Maesschalck, A. D., Waele, J. D., Lefever, T., Almey, R., Kwee, I., Zito, A., Deneweth, L., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.22.716296
Hossen, M. N. (2025) · Journal of Academic Biology and Biology Education · doi:10.37251/jouabe.v2i2.2323
Emergence of histone-based chromatin complexity in Asgard archaeaPreprint
Cho, C. H., Russett, C. S., Harvey, Z. H., Pende, N., Hodgskiss, L. H., Cangi, J., Radler, P., Hager, K., Homola, M., Imre, R., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.02.735847 · Cited by 1 · see citing works
- Authors
- Brunk, C. F., & Martin, W. F.
- Affiliations
- University of California, Los Angeles (US)
- Heinrich Heine University Düsseldorf (DE)
- Corresponding author
- Martin, William F.
- ORCID
- Martin, William F.
- Venue
- Trends in Microbiology
- Publisher
- Elsevier BV
- Published
- 2019-08
- Volume
- 27
- Issue
- 8
- Pages
- 703-714
- ISSN
- 0966-842X (ISSN-L)
- OpenAlex
- W2944327922
- Cited by
- 55
- References
- 109
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 14 · 2023: 1 · 2022: 9 · 2021: 8 · 2020: 10 · 2019: 3
- FWCI
- 0.66
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Trends in Microbiology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- Volkswagen Foundation
- European Research Council
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- archaeal histones, eukaryotic origin, endosymbiotic origin of eukaryotes, nucleosome, chromatin organization, epigenetic regulation, cell cycle, chromosome condensation, genome complexity, eukaryotic evolution
- MeSH terms
- Archaea, DNA, Eukaryotic Cells, Biological Evolution, Histones, Mitochondria, Symbiosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
