Cited by 155Protist diversity and phylogenyOrigins and Evolution of LifeEvolution and Genetic Dynamics

The DOI matches its Crossref record; 206 of the 206 references it cites were found in a registry or an index.

Symbiosis in eukaryotic evolution

Open access

López-García, Purificación, Eme, Laura, Moreira, David·2017·Journal of Theoretical Biology

DOI 10.1016/j.jtbi.2017.02.031PMC PMC5638015

Open this paper in CoChat — free account

Abstract

Fifty years ago, Lynn Margulis, inspiring in early twentieth-century ideas that put forward a symbiotic origin for some eukaryotic organelles, proposed a unified theory for the origin of the eukaryotic cell based on symbiosis as evolutionary mechanism. Margulis was profoundly aware of the importance of symbiosis in the natural microbial world and anticipated the evolutionary significance that integrated cooperative interactions might have as mechanism to increase cellular complexity. Today, we have started fully appreciating the vast extent of microbial diversity and the importance of syntrophic metabolic cooperation in natural ecosystems, especially in sediments and microbial mats. Also, not only the symbiogenetic origin of mitochondria and chloroplasts has been clearly demonstrated, but improvement in phylogenomic methods combined with recent discoveries of archaeal lineages more closely related to eukaryotes further support the symbiogenetic origin of the eukaryotic cell. Margulis left us in legacy the idea of 'eukaryogenesis by symbiogenesis'. Although this has been largely verified, when, where, and specifically how eukaryotic cells evolved are yet unclear. Here, we shortly review current knowledge about symbiotic interactions in the microbial world and their evolutionary impact, the status of eukaryogenetic models and the current challenges and perspectives ahead to reconstruct the evolutionary path to eukaryotes.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.jtbi.2017.02.031

Cites

206 of 206 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
Woese, C. R., Kandler, O., & Wheelis, M. L. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.12.4576 · Cited by 6,128
Phylogenetic structure of the prokaryotic domain: The primary kingdoms
Woese, C. R., & Fox, G. E. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.11.5088 · Cited by 4,131
Going back to the roots: the microbial ecology of the rhizosphere
Philippot, L., Raaijmakers, J. M., Lemanceau, P., & van der Putten, W. H. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3109 · Cited by 4,085
A marine microbial consortium apparently mediating anaerobic oxidation of methane
Boëtius, A., Ravenschlag, K., Schubert, C. J., Rickert, D., Widdel, F., Gieseke, A., Amann, R., Jørgensen, B. B., Witte, U. F. M., & Pfannkuche, O. (2000) · Nature · doi:10.1038/35036572 · Cited by 3,121
Evolutionary divergence and convergence in proteins.
ZUCKERKANDL, E., & PAULING, L. (1965) · Evolving Genes and Proteins · doi:10.1016/b978-1-4832-2734-4.50017-6 · Cited by 3,020
The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes
Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M., & Sessitsch, A. (2015) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00050-14 · Cited by 2,861
Wolbachia: master manipulators of invertebrate biology
Werren, J. H., Baldo, L., & Clark, M. E. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1969 · Cited by 2,830
The rise of oxygen in Earth's early ocean and atmosphere
Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014) · Nature · doi:10.1038/nature13068 · Cited by 2,810
A Molecular View of Microbial Diversity and the Biosphere
Pace, N. R. (1997) · Science · doi:10.1126/science.276.5313.734 · Cited by 2,797
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F. O., Ludwig, W., SCHLEIFER, K. H., Whitman, W. B., Euzéby, J. P., Amann, R., & Rossello-Mora, R. A. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3330 · Cited by 2,651
Insights into the phylogeny and coding potential of microbial dark matter
Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N. N., Anderson, I. J., Cheng, J.-F., Darling, A., Malfatti, S., Swan, B. K., Gies, E. A., et al. (2013) · Nature · doi:10.1038/nature12352 · Cited by 2,394
Diet–microbiota interactions as moderators of human metabolism
Sonnenburg, J. L., & Bäckhed, F. (2016) · Nature · doi:10.1038/nature18846 · Cited by 2,257
A new view of the tree of life
Hug, L. A., Baker, B. J., Anantharaman, K., Brown, C. T., Probst, A. J., Castelle, C. J., Butterfield, C. N., Hernsdorf, A. W., Amano, Y., Ise, K., et al. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.48 · Cited by 2,039
The microbiome and innate immunity
Thaiss, C. A., Zmora, N., Levy, M., & Elinav, E. (2016) · Nature · doi:10.1038/nature18847 · Cited by 2,012
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
The New Higher Level Classification of Eukaryotes with Emphasis on the Taxonomy of Protists
Adl, S., Simpson, A., Farmer, M. A., Andersen, R., Anderson, O., Barta, J. R., Bowser, S., Brugerolle, G., Fensome, R., Fredericq, S., et al. (2005) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.2005.00053.x · Cited by 1,749
The genome sequence of Rickettsia prowazekii and the origin of mitochondria
Andersson, S. G. E., Zomorodipour, A., Andersson, J. O., Sicheritz-Pontén, T., Alsmark, U. C. M., Podowski, R. M., Näslund, A. K., Eriksson, A.-S., Winkler, H. H., & Kurland, C. G. (1998) · Nature · doi:10.1038/24094 · Cited by 1,697
Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes
Timmis, J. N., Ayliffe, M., Huang, C. Y., & Martin, W. F. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1271 · Cited by 1,603
A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process
Lartillot, N., & Philippe, H. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh112 · Cited by 1,516
Extreme genome reduction in symbiotic bacteria
McCutcheon, J. P., & Moran, N. A. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2670 · Cited by 1,464
Symbiosis in cell evolution
Margulis, L. (1981) · Cited by 1,399
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
The Hydrogen Hypothesis for the First Eukaryote
Martin, W., & Müller, M. (1998) · Nature · doi:10.1038/32096 · Cited by 1,282
Asgard 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
Methane-Consuming Archaea Revealed by Directly Coupled Isotopic and Phylogenetic Analysis
Orphan, V. J., House, C. H., Hinrichs, K., McKeegan, K. D., & DeLong, E. F. (2001) · Science · doi:10.1126/science.1061338 · Cited by 1,101
Tracing the stepwise oxygenation of the Proterozoic ocean
Scott, C., Lyons, T. W., Bekker, A., Shen, Y., Poulton, S. W., Chu, X., & Anbar, A. D. (2008) · Nature · doi:10.1038/nature06811 · Cited by 1,098
Symbiotic diversity in marine animals: the art of harnessing chemosynthesis
Dubilier, N., Bergin, C., & Lott, C. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1992 · Cited by 1,073
The 1.2-Megabase Genome Sequence of Mimivirus
Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., Scola, B. L., Suzan, M., & Claverie, J. (2004) · Science · doi:10.1126/science.1101485 · Cited by 1,045
Spatial structure, cooperation and competition in biofilms
Nadell, C. D., Drescher, K., & Foster, K. R. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.84 · Cited by 1,012
Microbial syntrophy: interaction for the common good
Morris, B. E. L., Henneberger, R. M., Huber, H., & Moissl‐Eichinger, C. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12019 · Cited by 962
Estimating the timing of early eukaryotic diversification with multigene molecular clocks
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H., & Katz, L. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110633108 · Cited by 899
Eukaryotic evolution, changes and challenges
Embley, T. M., & Martin, W. (2006) · Nature · doi:10.1038/nature04546 · Cited by 867
Ancient Invasions: From Endosymbionts to Organelles
Dyall, S. D., Brown, M. T., & Johnson, P. J. (2004) · Science · doi:10.1126/science.1094884 · Cited by 847
Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes
Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R.-Y., van der Giezen, M., Tielens, A. G. M., & Martin, W. F. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05024-11 · Cited by 838
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics
Evans, P. N., Parks, D. H., Chadwick, G. L., Robbins, S. J., Orphan, V. J., Golding, S. D., & Tyson, G. W. (2015) · Science · doi:10.1126/science.aac7745 · Cited by 804
Gene transfer to the nucleus and the evolution of chloroplasts
Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M., & Kowallik, K. V. (1998) · Nature · doi:10.1038/30234 · Cited by 772
Wolbachia as a bacteriocyte-associated nutritional mutualist
Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X., & Fukatsu, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911476107 · Cited by 771
Evolving Genes and Proteins
(1965) · Elsevier eBooks · doi:10.1016/c2013-0-11981-2 · Cited by 747
Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru
Biddle, J. F., Lipp, J. S., Lever, M. A., Lloyd, K. G., Sørensen, K. B., Anderson, R. E., Fredricks, H. F., Elvert, M., Kelly, T. J., Schrag, D. P., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600035103 · Cited by 712
Eukaryotic organisms in Proterozoic oceans
Knoll, A. H., Javaux, E. J., Hewitt, D., & Cohen, P. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1843 · Cited by 701
Prokaryotic Cells in the Hydrothermal Vent Tube Worm Riftia pachyptila Jones: Possible Chemoautotrophic Symbionts
Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W., & Waterbury, J. B. (1981) · Science · doi:10.1126/science.213.4505.340 · Cited by 677
Methanobacillus omelianskii, a symbiotic association of two species of bacteria
Bryant, M. P., Wolin, E. A., Wolin, M. J., & WOLFE, R. S. (1967) · Archives of Microbiology · doi:10.1007/bf00406313 · Cited by 671
Genomic insights into the marine sponge microbiome
Hentschel, U., Piel, J., Degnan, S. M., & Taylor, M. W. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2839 · Cited by 659
Mitochondrial Evolution
Gray, M. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011403 · Cited by 639
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403984101 · Cited by 638
Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree 1 , 2
Cavalier-Smith, T. (1999) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.1999.tb04614.x · Cited by 633
Syntrophic exchange in synthetic microbial communities
Mee, M. T., Collins, J. J., Church, G. M., & Wang, H. H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405641111 · Cited by 619
The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology
Pester, M., Schleper, C., & Wagner, M. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.04.007 · Cited by 592
A molecular timescale of eukaryote evolution and the rise of complex multicellular life
Hedges, S. B., Blair, J. E., Venturi, M. L., & Shoe, J. L. (2004) · BMC Evolutionary Biology · doi:10.1186/1471-2148-4-2 · Cited by 578
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria
Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H. E., & Boëtius, A. (2015) · Nature · doi:10.1038/nature15733 · Cited by 568
Predominant archaea in marine sediments degrade detrital proteins
Lloyd, K. G., Schreiber, L., Petersen, D. G., Kjeldsen, K. U., Lever, M. A., Steen, A. D., Stepanauskas, R., Richter, M., Kleindienst, S., Lenk, S., et al. (2013) · Nature · doi:10.1038/nature12033 · Cited by 563
Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes
Rodríguez‐Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Löffelhardt, W., Bohnert, H. J., Philippe, H., & Lang, B. F. (2005) · Current Biology · doi:10.1016/j.cub.2005.06.040 · Cited by 559
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 546
Learning how to live together: genomic insights into prokaryote–animal symbioses
Moyá, A., Peretó, J. G., Gil, R., & Latorre, A. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2319 · Cited by 544
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation
Sieber, J. R., McInerney, M. J., & Gunsalus, R. P. (2010) · Annual Review of Microbiology · doi:10.1146/annurev-micro-090110-102844 · Cited by 541
Has the endosymbiont hypothesis been proven?
Gray, M. W., & Doolittle, W. F. (1982) · Microbiological Reviews · doi:10.1128/mr.46.1.1-42.1982 · Cited by 535
The Hologenome Concept: Helpful or Hollow?
Moran, N. A., & Sloan, D. B. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002311 · Cited by 533
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
Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts.
Schwartz, R. M., & Dayhoff, M. O. (1978) · Science · doi:10.1126/science.202030 · Cited by 508
Early evolution and the origin of eukaryotes
Sogin, M. L. (1991) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(05)80192-3 · Cited by 500
The Number, Speed, and Impact of Plastid Endosymbioses in Eukaryotic Evolution
Keeling, P. J. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120144 · Cited by 498
Syntrophy in anaerobic global carbon cycles
McInerney, M. J., Sieber, J. R., & Gunsalus, R. P. (2009) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2009.10.001 · Cited by 489
Untangling Genomes from Metagenomes: Revealing an Uncultured Class of Marine Euryarchaeota
Iverson, V., Morris, R. M., Frazar, C. D., Berthiaume, C. T., Morales, R. L., & Armbrust, E. V. (2012) · Science · doi:10.1126/science.1212665 · Cited by 475
The Puzzle of Plastid Evolution
Archibald, J. M. (2009) · Current Biology · doi:10.1016/j.cub.2008.11.067 · Cited by 469
Symbiosis insights through metagenomic analysis of a microbial consortium
Woyke, T., Teeling, H., Ivanova, N., Huntemann, M., Richter, M., Glöckner, F. O., Boffelli, D., Anderson, I., Barry, K., Shapiro, H., et al. (2006) · Nature · doi:10.1038/nature05192 · Cited by 462
A Eukaryote without a Mitochondrial Organelle
Karnkowska, A., Vacek, V., Zubáčová, Z., Treitli, S. C., Vargová, R., Eme, L., Novák, L., Žárský, V., Barlow, L. D., Herman, E. K., et al. (2016) · Current Biology · doi:10.1016/j.cub.2016.03.053 · Cited by 429
Self-citation
Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth
Schmid, R., Margulis, L., & Schwartz, K. V. (1988) · Taxon · doi:10.2307/1222104 · Cited by 419
Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism
McInerney, M. J., Struchtemeyer, C. G., Sieber, J. R., Mouttaki, H., Stams, A. J. M., Schink, B., Rohlin, L., & Gunsalus, R. P. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1419.005 · Cited by 406
Paleobiological Perspectives on Early Eukaryotic Evolution
Knoll, A. H. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016121 · Cited by 394
Components of Coated Vesicles and Nuclear Pore Complexes Share a Common Molecular Architecture
Devos, D. P., Dokudovskaya, S., Alber, F., Williams, R., Chait, B. T., Šali, A., & Rout, M. P. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020380 · Cited by 390
Happy together: microbial communities that hook up to swap electrons
Lovley, D. R. (2016) · The ISME Journal · doi:10.1038/ismej.2016.136 · Cited by 388
Rhizobium–legume symbioses: the crucial role of plant immunity
Gourion, B., Berrabah, F., Ratet, P., & Stacey, G. S. (2014) · Trends in Plant Science · doi:10.1016/j.tplants.2014.11.008 · Cited by 372
The archaeal ‘TACK’ superphylum and the origin of eukaryotes
Guy, L., & Ettema, T. J. G. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.09.002 · Cited by 372
The engine of the reef: photobiology of the coral–algal symbiosis
Roth, M. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00422 · Cited by 362
Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life.
Margulis, L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.3.1071 · Cited by 358
The tiniest tiny genomes.
Moran, N., & Bennett, G. (2014) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091213-112901 · Cited by 357
Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts
von Dohlen, C. D., Kohler, S., Alsop, S. T., & McManus, W. R. (2001) · Nature · doi:10.1038/35086563 · Cited by 353
A Small Microbial Genome: The End of a Long Symbiotic Relationship?
Pérez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M., Michelena, J. M., Silva, F. J., Moya, A., & Latorre, A. (2006) · Science · doi:10.1126/science.1130441 · Cited by 346
Algal ancestor of land plants was preadapted for symbiosis
Delaux, P., Radhakrishnan, G. V., Jayaraman, D., Cheema, J., Malbreil, M., Volkening, J. D., Sekimoto, H., Nishiyama, T., Melkonian, M., Pokorny, L., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515426112 · Cited by 326
Defining the Core Microbiome in Corals’ Microbial Soup
Hernández‐Agreda, A., Gates, R. D., & Ainsworth, T. D. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.11.003 · Cited by 326
Symbiosis Between Methanogenic Archaea and δ-Proteobacteria as the Origin of Eukaryotes: The Syntrophic Hypothesis
Moreira, D., & López‐García, P. (1998) · Journal of Molecular Evolution · doi:10.1007/pl00006408 · Cited by 324
Self-citation
The early evolution of lipid membranes and the three domains of life
Lombard, J., López-García, P., & Moreira, D. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2815 · Cited by 320
Self-citation
Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge
Jørgensen, S. L., Hannisdal, B., Lanzén, A., Baumberger, T., Flesland, K., Fonseca, R., Øvreås, L., Steen, I. H., Thorseth, I. H., Pedersen, R. B., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207574109 · Cited by 318
Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits
Javaux, E., Marshall, C. P., & Bekker, A. (2010) · Nature · doi:10.1038/nature08793 · Cited by 307
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
Precision of molecular time estimates
Hedges, S. B., & Kumar, S. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.03.004 · Cited by 292
The Genotypic View of Social Interactions in Microbial Communities
Mitri, S., & Foster, K. R. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133307 · Cited by 291
Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics
Pernthaler, A., Dekas, A., Brown, C. T., Goffredi, S. K., Embaye, T., & Orphan, V. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711303105 · Cited by 288
The molecular ecology of microbial eukaryotes unveils a hidden world
Moreira, D., & López‐García, P. (2002) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02257-0 · Cited by 288
Self-citation
On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks
Eme, L., Sharpe, S. C., Brown, M. W., & Roger, A. J. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016139 · Cited by 287
Self-citation
Reconstructing Early Events in Eukaryotic Evolution
Roger, A. J. (1999) · The American Naturalist · doi:10.1086/303290 · Cited by 283
Has the endosymbiont hypothesis been proven?
Gray, M. W., & Doolittle, W. F. (1982) · Microbiological Reviews · doi:10.1128/mmbr.46.1.1-42.1982 · Cited by 282
Single-cell genomics reveals the lifestyle of Poribacteria , a candidate phylum symbiotically associated with marine sponges
Siegl, A., Kamke, J., Hochmuth, T., Piel, J., Richter, M., Liang, C., Dandekar, T., & Hentschel, U. (2011) · The ISME Journal · doi:10.1038/ismej.2010.95 · Cited by 276
An early-branching freshwater cyanobacterium at the origin of plastids
Ponce-Toledo, R. I., Deschamps, P., López-García, P., Zivanovic, Y., Benzerara, K., & Moreira, D. (2017) · Current Biology · doi:10.1016/j.cub.2016.11.056 · Cited by 274
Self-citation
The origin of eukaryotes: a reappraisal
Duve, C. D. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2071 · Cited by 273
Early branching eukaryotes?
Embley, T. M., & Hirt, R. P. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80029-4 · Cited by 272
The impact of endosymbionts on the evolution of host sex-determination mechanisms
Cordaux, R., Bouchon, D., & Grève, P. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.05.002 · Cited by 271
The Santa Barbara Basin is a symbiosis oasis
Bernhard, J. M., Buck, K. R., Farmer, M. A., & Bowser, S. S. (2000) · Nature · doi:10.1038/47476 · Cited by 270
Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry
Pittis, A. A., & Gabaldón, T. (2016) · Nature · doi:10.1038/nature16941 · Cited by 259
Networks of energetic and metabolic interactions define dynamics in microbial communities
Embree, M., Liu, J. K., Al-Bassam, M. M., & Zengler, K. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506034112 · Cited by 256
Rapid evolution of stability and productivity at the origin of a microbial mutualism
Hillesland, K. L., & Stahl, D. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908456107 · Cited by 254
Phylogenomic Evidence for Separate Acquisition of Plastids in Cryptophytes, Haptophytes, and Stramenopiles
Baurain, D., Brinkmann, H., Petersen, J., Rodríguez‐Ezpeleta, N., Stechmann, A., Demoulin, V., Roger, A. J., Burger, G., Lang, B. F., & Philippe, H. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq059 · Cited by 254
Early–branching or fast–evolving eukaryotes? An answer based on slowly evolving positions
Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M., & Guyader, H. L. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1130 · Cited by 247
Self-citation
The origin of red algae and the evolution of chloroplasts
Moreira, D., le Guyader, H., & Philippe, H. (2000) · Nature · doi:10.1038/35011054 · Cited by 245
Self-citation
Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis
Husník, F., & McCutcheon, J. P. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603910113 · Cited by 245
Metabolic symbiosis at the origin of eukaryotes
López‐García, P., & Moreira, D. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(98)01342-5 · Cited by 244
Self-citation
Endosymbiotic associations within protists
Nowack, E., & Melkonian, M. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2009.0188 · Cited by 239
Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat
Harris, J. K., Caporaso, J. G., Walker, J. J., Spear, J. R., Gold, N. J., Robertson, C. E., Hugenholtz, P., Goodrich, J. K., McDonald, D. T., Knights, D., et al. (2012) · The ISME Journal · doi:10.1038/ismej.2012.79 · Cited by 236
The chimeric eukaryote: Origin of the nucleus from the karyomastigont in amitochondriate protists
Margulis, L., Dolan, M. F., & Guerrero, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.13.6954 · Cited by 233
Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea
Sathi, S. N., Dagan, T., Landan, G., Janssen, A., Steel, M., McInerney, J. O., Deppenmeier, U., & Martin, W. F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209119109 · Cited by 226
The origins of plastids
Cavalier‐Smith, T. (1982) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.1982.tb02023.x · Cited by 223
Symbiogenesis: the holobiont as a unit of evolution.
Guerrero, R., Margulis, L., & Berlanga, M. (2013) · PubMed · doi:10.2436/20.1501.01.188 · Cited by 219
‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle
Sassera, D., Beninati, T., Bandi, C., Bouman, E. A. P., Sacchi, L., Fabbi, M., & Lo, N. C. (2006) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.64386-0 · Cited by 215
A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record
Berney, C., & Pawlowski, J. (2006) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2006.3537 · Cited by 212
Symbiotic options for the conquest of land
Field, K. J., Pressel, S., Duckett, J. G., Rimington, W. R., & Bidartondo, M. I. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.05.007 · Cited by 211
Methane as Fuel for Anaerobic Microorganisms
Thauer, R. K., & Shima, S. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1419.000 · Cited by 209
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia
Hatzenpichler, R., Connon, S. A., Goudeau, D., Malmstrom, R. R., Woyke, T., & Orphan, V. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603757113 · Cited by 206
The last eukaryotic common ancestor (LECA): Acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon
Margulis, L., Chapman, M., Guerrero, R., & Hall, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604985103 · Cited by 201
Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen
Mereschkowsky, C. (1910) · Medical Entomology and Zoology · Cited by 200
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 196
Protist classification and the kingdoms of organisms
WHITTAKER, R. H., & Margulis, L. (1978) · Biosystems · doi:10.1016/0303-2647(78)90023-0 · Cited by 192
Phylogenetic and Phyletic Studies of Informational Genes in Genomes Highlight Existence of a 4th Domain of Life Including Giant Viruses
Boyer, M., Madoui, M., Gimenez, G., Scola, B. L., & Raoult, D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015530 · Cited by 190
Symbionticism and the Origin of Species.
(1927) · JAMA · doi:10.1001/jama.1927.02680460059034 · Cited by 189
The origin of plastids
Howe, C. J., Barbrook, A. C., Nisbet, R. E. R., Lockhart, P. J., & Larkum, A. W. D. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0050 · Cited by 186
The Deep Archaeal Roots of Eukaryotes
Yutin, N., Makarova, K. S., Mekhedov, S., Wolf, Y. I., & Koonin, E. V. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn108 · Cited by 184
The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation
Roger, A. J., & Hug, L. A. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1845 · Cited by 180
An Evolutionary Network of Genes Present in the Eukaryote Common Ancestor Polls Genomes on Eukaryotic and Mitochondrial Origin
Thiergart, T., Landan, G., Schenk, M., Dagan, T., & Martin, W. F. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs018 · Cited by 174
The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse?
Gribaldo, S., Poole, A. M., Daubin, V., Forterre, P., & Brochier‐Armanet, C. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2426 · Cited by 173
Evaluating hypotheses for the origin of eukaryotes.
Poole, A. M., & Penny, D. (2007) · Bioessays · doi:10.1002/bies.20516 · Cited by 156
Experimental evolution in biofilm populations
Steenackers, H. P. L., Parijs, I., Foster, K. R., & Vanderleyden, J. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw002 · Cited by 156
A congruent phylogenomic signal places eukaryotes within the Archaea
Williams, T. A., Foster, P. G., Nye, T. M. W., Cox, C. J., & Embley, T. M. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1795 · Cited by 153
The oldest records of photosynthesis
Awramik, S. M. (1992) · Photosynthesis Research · doi:10.1007/bf00039172 · Cited by 151
Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont
Koga, R., & Moran, N. A. (2014) · The ISME Journal · doi:10.1038/ismej.2013.235 · Cited by 151
Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea
Baker, B. J., Saw, J. H. W., Lind, A. E., Lazar, C. S., Hinrichs, K., Teske, A., & Ettema, T. J. G. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.2 · Cited by 151
Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics
Robidart, J. C., Bench, S. R., Feldman, R. A., Novoradovsky, A., Podell, S. B., Gaasterland, T., Allen, E. E., & Felbeck, H. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01496.x · Cited by 146
Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico
Duperron, S., Sibuet, M., MacGregor, B. J., Kuypers, M. M. M., Fisher, C. R., & Dubilier, N. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2007.01259.x · Cited by 146
Mutualism and parasitism: the yin and yang of plant symbioses
Paszkowski, U. (2006) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2006.05.008 · Cited by 145
Experimental replacement of an obligate insect symbiont
Moran, N. A., & Yun, Y. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420037112 · Cited by 145
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 141
Selective forces for the origin of the eukaryotic nucleus
López‐García, P., & Moreira, D. (2006) · BioEssays · doi:10.1002/bies.20413 · Cited by 138
Self-citation
Small GTPases and the evolution of the eukaryotic cell
Jékely, G. (2003) · BioEssays · doi:10.1002/bies.10353 · Cited by 137
Open Questions on the Origin of Eukaryotes
López-García, P., & Moreira, D. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.09.005 · Cited by 135
Self-citation
Five kingdoms: an illustrated guide to the phyla of life on Earth
(1998) · Choice Reviews Online · doi:10.5860/choice.35-6205 · Cited by 132
Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane
Wegener, G., Krukenberg, V., Ruff, S. E., Kellermann, M. Y., & Knittel, K. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00046 · Cited by 127
From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell
Martijn, J., & Ettema, T. J. G. (2013) · Biochemical Society Transactions · doi:10.1042/bst20120292 · Cited by 126
Lokiarchaeon is hydrogen dependent
Sousa, F. L., Neukirchen, S., Allen, J. F., Lane, N. J., & Martin, W. F. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.34 · Cited by 126
Multiple secondary origins of the anaerobic lifestyle in eukaryotes
Martin Embley, T. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1844 · Cited by 124
Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome
Leclercq, S., Thézé, J., Chebbi, M. A., Giraud, I., Moumen, B., Ernenwein, L., Grève, P., Gilbert, C., & Cordaux, R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1608979113 · Cited by 123
Archaebacteria and Archezoa
Cavalier‐Smith, T. (1989) · Nature · doi:10.1038/339100a0 · Cited by 119
Microbial interactions involving sulfur bacteria: implications for the ecology and evolution of bacterial communities
Overmann, J., & van Gemerden, H. (2000) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2000.tb00560.x · Cited by 119
Bacterial gene import and mesophilic adaptation in archaea
López‐García, P., Zivanovic, Y., Deschamps, P., & Moreira, D. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3485 · Cited by 115
Self-citation
Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park
Kozubal, M. A., Romine, M. F., Jennings, R. D., Jay, Z. J., Tringe, S. G., Rusch, D. B., Beam, J. P., McCue, L. A., & Inskeep, W. P. (2012) · The ISME Journal · doi:10.1038/ismej.2012.132 · Cited by 114
The origins and early evolution of DNA mismatch repair genes—multiple horizontal gene transfers and co-evolution
Lin, Z., Nei, M., & Mā, H. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm921 · Cited by 113
Giant viruses and the origin of modern eukaryotes
Forterre, P., & Gaïa, M. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2016.02.001 · Cited by 110
Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora.
Nakayama, T., & Ishida, K. (2009) · Current Biology · doi:10.1016/j.cub.2009.02.043 · Cited by 103
Archaeal “Dark Matter” and the Origin of Eukaryotes
Williams, T. A., & Embley, T. M. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu031 · Cited by 103
Pangenome Evidence for Extensive Interdomain Horizontal Transfer Affecting Lineage Core and Shell Genes in Uncultured Planktonic Thaumarchaeota and Euryarchaeota
Deschamps, P., Zivanovic, Y., Moreira, D., Rodríguez‐Valera, F., & López‐García, P. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu127 · Cited by 101
Self-citation
The Origin and Evolution of The Cell
(1993) · doi:10.1142/1909 · Cited by 101
Tracing the Archaeal Origins of Eukaryotic Membrane-Trafficking System Building Blocks
Klinger, C. M., Spang, A., Dacks, J. B., & Ettema, T. J. G. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw034 · Cited by 98
Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the ‘lipid divide’
Villanueva, L., Stefan Schouten, A., & Damsté, J. S. S. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13361 · Cited by 98
Cellular cooperation: insights from microbes
Celiker, H., & Gore, J. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.08.010 · Cited by 94
What Does It Take to Evolve A Nitrogen-Fixing Endosymbiosis?
Geurts, R., Xiao, T. T., & Reinhold‐Hurek, B. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.01.012 · Cited by 94
Unusual Butane- and Pentanetriol-Based Tetraether Lipids in Methanomassiliicoccus luminyensis, a Representative of the Seventh Order of Methanogens
Becker, K. W., Elling, F. J., Yoshinaga, M. Y., Söllinger, A., Urich, T., & Hinrichs, K. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.00772-16 · Cited by 90
Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A
Zehr, J., Shilova, I., Farnelid, H., Muñoz-Marín, M. D. C., & Turk-Kubo, K. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.214 · Cited by 90
Advances in Time Estimation Methods for Molecular Data
Kumar, S., & Hedges, S. B. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw026 · Cited by 88
Informational Gene Phylogenies Do Not Support a Fourth Domain of Life for Nucleocytoplasmic Large DNA Viruses
Williams, T. A., Embley, T. M., & Heinz, E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021080 · Cited by 87
Evolutionary Transitions to Multicellular Life
Ruiz‐Trillo, I., & Nedelcu, A. M. (2015) · Advances in marine genomics · doi:10.1007/978-94-017-9642-2 · Cited by 87
Metagenomics of the subsurface Brazos-Trinity Basin (IODP site 1320): comparison with other sediment and pyrosequenced metagenomes
Biddle, J. F., White, J. R., Teske, A., & House, C. H. (2011) · The ISME Journal · doi:10.1038/ismej.2010.199 · Cited by 86
BIOCHEMISTRY OF PROTOZOAN MICROBODIES: Peroxisomes, α-Glycerophosphate Oxidase Bodies, Hydrogenosomes
Müller, M. (1975) · Annual Review of Microbiology · doi:10.1146/annurev.mi.29.100175.002343 · Cited by 85
Comment on "The 1.2-Megabase Genome Sequence of Mimivirus"
Moreira, D., & López‐García, P. (2005) · Science · doi:10.1126/science.1110820 · Cited by 83
Self-citation
Environmental Breviatea harbour mutualistic Arcobacter epibionts
Hamann, E., Gruber‐Vodicka, H. R., Kleiner, M., Tegetmeyer, H. E., Riedel, D., Littmann, S., Chen, J., Milucka, J., Viehweger, B., Becker, K. W., et al. (2016) · Nature · doi:10.1038/nature18297 · Cited by 81
Wheat embryo mitochondrial 18S ribosomal RNA: evidence for its prokaryotic nature
Bonen, L., Cunningham, R. S., Gray, M. W., & Doolittle, W. F. (1977) · Nucleic Acids Research · doi:10.1093/nar/4.3.663 · Cited by 80
Paleobiological Perspectives on Early Microbial EvolutionPreprint
Knoll, A. H. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018093 · Cited by 78
Rethinking “mutualism” in diverse host‐symbiont communities
Mushegian, A. A., & Ebert, D. (2015) · BioEssays · doi:10.1002/bies.201500074 · Cited by 77
Novel mitochondrion‐related organelles in the anaerobic amoeba Mastigamoeba balamuthi
Gill, E. E., Trivino, S. D., Barberà, M. J., Silberman, J. D., Stechmann, A., Gaston, D., Tamaš, I., & Roger, A. J. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05979.x · Cited by 76
Methods for unveiling cryptic microbial partnerships in nature
Orphan, V. J. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.04.003 · Cited by 73
The Early Eukaryotic Fossil Record
Javaux, E. (2008) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-74021-8_1 · Cited by 72
How Really Ancient Is Paulinella Chromatophora?
Delaye, L., Valadez-Cano, C., & Pérez-Zamorano, B. (2016) · PLoS Currents · doi:10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b · Cited by 72
Endosymbiosis and its implications for evolutionary theory
O’Malley, M. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421389112 · Cited by 69
Archaeal ancestors of eukaryotes: not so elusive any more
Koonin, E. V. (2015) · BMC Biology · doi:10.1186/s12915-015-0194-5 · Cited by 68
Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
Noda, S., Hongoh, Y., Sato, T., & Ohkuma, M. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-158 · Cited by 68
Structured Multiple Endosymbiosis of Bacteria and Archaea in a Ciliate from Marine Sulfidic Sediments: A Survival Mechanism in Low Oxygen, Sulfidic Sediments?
Edgcomb, V. P., Leadbetter, E. R., Bourland, W. A., Beaudoin, D., & Bernhard, J. M. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00055 · Cited by 67
The Neomuran Revolution and Phagotrophic Origin of Eukaryotes and Cilia in the Light of Intracellular Coevolution and a Revised Tree of LifePreprint
Cavalier‐Smith, T. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016006 · Cited by 67
Time‐dependent estimates of molecular evolutionary rates: evidence and causes
Ho, S. Y. W., Duchêne, S., Molak, M., & Shapiro, B. (2015) · Molecular Ecology · doi:10.1111/mec.13450 · Cited by 60
The Impact of History on Our Perception of Evolutionary Events: Endosymbiosis and the Origin of Eukaryotic ComplexityPreprint
Keeling, P. J. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016196 · Cited by 58
Quantitative and phylogenetic study of the Deep Sea Archaeal Group in sediments of the Arctic mid-ocean spreading ridge
Jørgensen, S. L., Thorseth, I. H., Pedersen, R. B., Baumberger, T., & Schleper, C. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00299 · Cited by 54
Response to Comment on "The 1.2-Megabase Genome Sequence of Mimivirus"
Ogata, H., Abergel, C., Raoult, D., & Claverie, J. (2005) · Science · doi:10.1126/science.1111195 · Cited by 51
Timing the Origins of Multicellular Eukaryotes Through Phylogenomics and Relaxed Molecular Clock Analyses
Sharpe*, S. C., Eme*, L., Brown, M. W., & Roger, A. J. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_1 · Cited by 49
Self-citation
Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution
Edgcomb, V. P., Breglia, S. A., Naoji Yubuki, A., Beaudoin, D., Patterson, D. J., Leander, B. S., & Bernhard, J. M. (2010) · The ISME Journal · doi:10.1038/ismej.2010.121 · Cited by 49
Biodiversity: molecular biological domains, symbiosis and kingdom origins
Margulis, L. (1992) · Biosystems · doi:10.1016/0303-2647(92)90045-z · Cited by 44
Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum”
Liu, Z., Müller, J., Li, T., Alvey, R. M., Vogl, K., Frigaard, N., Rockwell, N. C., Boyd, E. S., Tomsho, L. P., Schuster, S. C., et al. (2013) · Genome biology · doi:10.1186/gb-2013-14-11-r127 · Cited by 44
An integrated study reveals diverse methanogens, Thaumarchaeota, and yet-uncultivated archaeal lineages in Armenian hot springs
Hedlund, B. P., Dodsworth, J. A., Cole, J. K., & Panosyan, H. (2013) · Antonie van Leeuwenhoek · doi:10.1007/s10482-013-9927-z · Cited by 43
A New Era of Methanogenesis Research
Lever, M. A. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2015.12.005 · Cited by 40
The Viral Eukaryogenesis Hypothesis
Bell, P. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04994.x · Cited by 35
A life history view of mutualistic viral symbioses: quantity or quality for cooperation?
Bao, X., & Roossinck, M. J. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.05.007 · Cited by 32
What Was the Real Contribution of Endosymbionts to the Eukaryotic Nucleus? Insights from Photosynthetic EukaryotesPreprint
Moreira, D., & Deschamps, P. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016014 · Cited by 32
Self-citation
Sure facts and open questions about the origin and evolution of photosynthetic plastids
Moreira, D., & Philippe, H. (2001) · Research in Microbiology · doi:10.1016/s0923-2508(01)01260-8 · Cited by 32
Self-citation
Kingdoms in turmoil.
Margulis, L., & Guerrero, R. (1991) · PubMed · Cited by 29
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
Changing ideas about eukaryotic origins
Williams, T. A., & Embley, T. M. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0318 · Cited by 27

Flagged first, then by citations

Research works printed but not linked: 3

Cavalier-Smith, 1989, Molecular phylogeny, Archaebacteria Archezoa. Nat., 339, l00
Mereschkowsky, 1905, Über natur und usprung der chromatophoren im pflanzenreiche, Biol. Cent., 25, 593
Yan, 1993, Significance of eukaryotic organisms in the microfossil flora of Changcheng system, Acta Micropalaeontol Sin., 10, 167

Sorted by citations

BlobToolKit – Interactive Quality Assessment of Genome Assemblies
CHALLIS, R. J., Richards, E., Rajan, J., Cochrane, G., & Blaxter, M. (2020) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400908 · Cited by 2,600
The Origin and Diversification of Mitochondria
Roger, A. J., Muñoz-Gómez, S. A., & Kamikawa, R. (2017) · Current Biology · doi:10.1016/j.cub.2017.09.015 · Cited by 1,142
Soil protists: a fertile frontier in soil biology research
Geisen, S., Mitchell, E. A. D., Adl, S. M., Bonkowski, M., Dunthorn, M., Ekelund, F., Fernández, L. D., Jousset, A., Krashevska, V., Singer, D., et al. (2018) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuy006 · Cited by 756
Probiotics, Prebiotics, and Phytogenic Substances for Optimizing Gut Health in Poultry
Shehata, A. A., Yalçın, S., Latorre, J. D., Basiouni, S., Attia, Y. A., El‐Wahab, A. A., Visscher, C., El-Seedi, H. R., Huber, C., Hafez, H. M., et al. (2022) · Microorganisms · doi:10.3390/microorganisms10020395 · Cited by 329
Origin of viruses: primordial replicators recruiting capsids from hosts
Krupovìč, M., Dolja, V. V., & Koonin, E. V. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0205-6 · Cited by 213

See all 155

Authors: López-García, P., Eme, L., & Moreira, D.
Affiliations: Dalhousie University (CA)
Université Paris-Sud (FR)
ORCID: Eme, Laura
Moreira, David
Venue: Journal of Theoretical Biology
Publisher: Elsevier BV
Published: 2017-12
Volume: 434
Pages: 20-33
ISSN: 0022-5193 (ISSN-L)
DOI: 10.1016/j.jtbi.2017.02.031
PMC: PMC5638015
OpenAlex: W2592590328
Cited by: 154
References: 206
Citations by year: 2026: 8 · 2025: 14 · 2024: 12 · 2023: 14 · 2022: 15 · 2021: 18 · 2020: 24 · 2019: 24 · 2018: 13 · 2017: 12
FWCI: 8.16
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Theoretical Biology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: European Research Council Advanced (322669)
Topics: Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
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
Keywords: symbiosis, eukaryotic origin, symbiogenesis, Lynn Margulis, endosymbiotic origin of mitochondria, chloroplast origin, eukaryotic organelles, microbial mats, sediment microbial communities, archaea, phylogenomics, eukaryotic evolution
MeSH terms: Eukaryotic Cells, Biological Evolution, Symbiosis, Ecosystem, Eukaryota, Microbiota

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

Symbiosis in eukaryotic evolution

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks