Symbiogenesis

File:Konstantin Mereschkowski Symbiogenesis Tree of Life.jpg's 1905 tree-of-life diagram, showing the origin of complex life-forms by two episodes of symbiogenesis, the incorporation of symbiotic bacteria to form successively nuclei and chloroplasts{{cite magazine |title=Mereschkowsky's Tree of Life |url=https://www.scientificamerican.com/article/mereschkowskys-tree-of-li/# |magazine=Scientific American |access-date=1 May 2017}}]]

The Russian botanist Konstantin Mereschkowski first outlined the theory of symbiogenesis (from Greek: σύν syn "together", βίος bios "life", and γένεσις genesis "origin, birth") in his 1905 work, The nature and origins of chromatophores in the plant kingdom, and then elaborated it in his 1910 The Theory of Two Plasms as the Basis of Symbiogenesis, a New Study of the Origins of Organisms.{{cite journal |last=Mereschkowski |first=Konstantin |author-link=Konstantin Mereschkowski |title=Über Natur und Ursprung der Chromatophoren im Pflanzenreiche |trans-title=On the nature and origin of chromatophores in the plant kingdom |journal=Biologisches Centralblatt |date=15 September 1905 |volume=25 |issue=18 |pages=593–604 |language=de |url=https://babel.hathitrust.org/cgi/pt?id=uc1.31822009245838;view=1up;seq=603}}See:

• {{cite journal |last=Mereschkowski |first=Konstantin |title=Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen |journal=Biologisches Centralblatt |date=15 April 1910 |volume=30 |issue=8 |pages=278–288 |url=https://babel.hathitrust.org/cgi/pt?id=uc1.31822009245903;view=1up;seq=292 |trans-title=Theory of two types of plasms as the basis of symbiogenesis, a new study of the origin of organisms [part 1 of 4] |language=de |ref=none}}
• {{cite journal |last=Mereschkowsky |first=Konstantin |title=Theorie der zwei Plasmaarten als Grundlage der Symbogenesis, einer neuen Lehre von der Entstehung der Organismen |journal=Biologisches Centralblatt |date=1 May 1910 |volume=30 |issue=9 |pages=289–303 |url=https://babel.hathitrust.org/cgi/pt?id=uc1.31822009245903;view=1up;seq=303 |trans-title=Theory of two types of plasms as the basis of symbiogenesis, a new study of the origin of organisms [part 2 of 4] |language=de |ref=none}}
• {{cite journal |last=Mereschkowski |first=Konstantin |title=Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen |journal=Biologisches Centralblatt |date=15 May 1910 |volume=30 |issue=10 |pages=321–347 |url=https://babel.hathitrust.org/cgi/pt?id=uc1.31822009245903;view=1up;seq=335 |trans-title=Theory of two types of plasms as the basis of symbiogenesis, a new study of the origin of organisms [part 3 of 4] |language=de |ref=none}}
• {{cite journal |last=Mereschkowsky |first=Konstantin |title=Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen |trans-title=Theory of two types of plasms as the basis of symbiogenesis, a new study of the origin of organisms [part 4 of 4] |journal=Biologisches Centralblatt |date=1 June 1910 |volume=30 |issue=11 |pages=353–367 |language=de |url=https://babel.hathitrust.org/cgi/pt?id=uc1.31822009245903;view=1up;seq=367 |ref=none}}{{cite journal |last1=Martin |first1=William F. |author1-link=William F. Martin |last2=Roettger |first2=Mayo |last3=Kloesges |first3=Thorsten |last4=Thiergart |first4=Thorsten |last5=Woehle |first5=Christian |last6=Gould |first6=Sven |last7=Dagan |first7=Tal |display-authors=3 |title=Modern endosymbiotic theory: Getting lateral gene transfer into the equation |url=http://www.molevol.hhu.de/fileadmin/redaktion/Fakultaeten/Mathematisch-Naturwissenschaftliche_Fakultaet/Biologie/Institute/Molekulare_Evolution/Dokumente/martin001.pdf |url-status=dead |journal=Journal of Endocytobiosis and Cell Research |volume=23 |pages=1–5 |archive-url=https://web.archive.org/web/20220309044351/https://www.molevol.hhu.de/fileadmin/redaktion/Fakultaeten/Mathematisch-Naturwissenschaftliche_Fakultaet/Biologie/Institute/Molekulare_Evolution/Dokumente/martin001.pdf |archive-date=2022-03-09 |access-date=2015-07-20}}(journal URL: [http://www.molevol.hhu.de/fileadmin/redaktion/Fakultaeten/Mathematisch-Naturwissenschaftliche_Fakultaet/Biologie/Institute/Molekulare_Evolution/Dokumente/martin001.pdf] {{Webarchive|url=https://web.archive.org/web/20220309044351/https://www.molevol.hhu.de/fileadmin/redaktion/Fakultaeten/Mathematisch-Naturwissenschaftliche_Fakultaet/Biologie/Institute/Molekulare_Evolution/Dokumente/martin001.pdf|date=2022-03-09}}) Mereschkowski proposed that complex life-forms had originated by two episodes of symbiogenesis, the incorporation of symbiotic bacteria to form successively nuclei and chloroplasts. Mereschkowski knew of the work of botanist Andreas Schimper. In 1883, Schimper had observed that the division of chloroplasts in green plants closely resembled that of free-living cyanobacteria. Schimper had tentatively proposed (in a footnote) that green plants had arisen from a symbiotic union of two organisms.See:
• {{cite journal |last=Schimper |first=A. F. W. |title=Ueber die Entwicklung der Chlorophyllkörner und Farbkörper |journal=Botanische Zeitung |date=16 February 1883 |volume=41 |issue=7 |pages=105–114 |url=https://babel.hathitrust.org/cgi/pt?id=hvd.32044106391576;view=1up;seq=91 |trans-title=On the development of chlorophyll granules and colored bodies [part 1 of 4] |language=de |ref=none}} From p. 105: "Inzwischen theilte mir Herr Professor Schmitz mit, dass … die höheren Pflanzen sich ebenso verhalten würden." (Meanwhile, Prof. Schmitz reported to me that among algae, the creation of chlorophyll granules from the cell plasm doesn't occur, but that they arise exclusively from one another by division. The spores receive from the mother plant chlorophyll granules, which create, by division, all of the chlorophyll granules of the plants that arises from them [i.e., the spores]. This finding in algae made it seem likely to Prof. Schmitz that the higher plants would behave likewise.) From p. 106: "Meine Untersuchungen haben ergeben, … aus dem Scheitelmeristem sich entwickelnden Gewebe erzeugen." (My investigations have revealed that the vegetation points [i.e., points of vegetative growth] always contain differentiated chlorophyll bodies or their colorless rudiments; that they arise not by creation from the cell plasm, but from one another by division, and that they create all chlorophyll bodies and starch-forming [bodies] of the tissues developing from the apical meristem.) From p. 112, footnote 2: "Sollte es sich definitiv bestätigen, … an eine Symbiose erinnern." (If it should definitely be confirmed that the plastids in egg cells are not formed anew, then their relation to the organism containing them would somewhat suggest a symbiosis.)
• {{cite journal |last=Schimper |first=A. F. W. |title=Ueber die Entwicklung der Chlorophyllkörner und Farbkörper |journal=Botanische Zeitung |date=23 February 1883 |volume=41 |issue=8 |pages=121–131 |url=https://babel.hathitrust.org/cgi/pt?id=hvd.32044106391576;view=1up;seq=99 |trans-title=On the development of chlorophyll granules and colored bodies [part 2 of 4] |language=de |ref=none}}
• {{cite journal |last=Schimper |first=A. F. W. |title=Ueber die Entwicklung der Chlorophyllkörner und Farbkörper |journal=Botanische Zeitung |date=2 March 1883 |volume=41 |issue=9 |pages=137–146 |url=https://babel.hathitrust.org/cgi/pt?id=hvd.32044106391576;view=1up;seq=107 |trans-title=On the development of chlorophyll granules and colored bodies [part 3 of 4] |language=de |ref=none}}
• {{cite journal |last=Schimper |first=A. F. W. |title=Ueber die Entwicklung der Chlorophyllkörner und Farbkörper |journal=Botanische Zeitung |date=9 March 1883 |volume=41 |issue=10 |pages=153–162 |url=https://babel.hathitrust.org/cgi/pt?id=hvd.32044106391576;view=1up;seq=115 |trans-title=On the development of chlorophyll granules and colored bodies [part 4 of 4] |language=de |ref=none}} In 1918 the French scientist Paul Jules Portier published Les Symbiotes, in which he claimed that the mitochondria originated from a symbiosis process.{{cite book |last=Portier |first=Paul |title=Les Symbiotes |date=1918 |publisher=Masson et Cie. |location=Paris, France |page=293 |url=https://babel.hathitrust.org/cgi/pt?id=mdp.39015011399261;view=1up;seq=325 |language=fr}} From p. 293: "Cette modification dans les rapports des appareils nucléaire et mitochondrial peut être le résultat de deux mécanismes. … Cette la parthénogénèse." (This modification in the relations of the nuclear and mitochondrial systems could be the result of two mechanisms: (a) There is a combination of two factors: contribution of new symbionts by the spermatozoid and reduction division. That is fertilization. (b) A single factor exists: reduction division: in this case, the egg contains sufficiently active symbionts. That is parthenogenesis.){{cite book |last=Lane |first=Nick |author-link=Nick Lane |title=Power, Sex, Suicide. Mitochondria and the Meaning of Life |url=https://archive.org/details/powersexsuicidem0000lane |url-access=registration |date=2005 |publisher=Oxford University Press |location=New York |isbn=9780199205646 |page=[https://archive.org/details/powersexsuicidem0000lane/page/14 14]}} Ivan Wallin advocated the idea of an endosymbiotic origin of mitochondria in the 1920s.{{cite journal |last=Wallin |first=Ivan E. |author-link=Ivan Wallin |title=The Mitochondria Problem |journal=The American Naturalist |year=1923 |volume=57 |issue=650 |pages=255–61 |doi=10.1086/279919|bibcode=1923ANat...57..255W |s2cid=85144224 }}{{cite book |last=Wallin |first=Ivan E. |author-link=Ivan Wallin |title=Symbionticism and the origin of species |year=1927 |publisher=Williams & Wilkins |location=Baltimore |pages=117 |url=https://archive.org/stream/symbionticismori00wall#page/116/mode/2up}}

The Russian botanist Boris Kozo-Polyansky became the first to explain the theory in terms of Darwinian evolution.{{cite journal |last=Margulis |first=Lynn |author-link=Lynn Margulis |title=Symbiogenesis. A new principle of evolution rediscovery of Boris Mikhaylovich Kozo-Polyansky (1890–1957) |journal=Paleontological Journal |year=2011 |volume=44 |issue=12 |pages=1525–1539 |doi=10.1134/S0031030110120087|s2cid=86279772 |url=https://works.bepress.com/cgi/viewcontent.cgi?article=1019&context=lynn_margulis }} In his 1924 book A New Principle of Biology. Essay on the Theory of Symbiogenesis,{{cite book |last=Kozo-Polyansky |first=Boris Mikhaylovich |title=Новый принцип биологии. Очерк теории симбиогенеза |trans-title=A New Principle of Biology. Essay on the Theory of Symbiogenesis |date=1924 |publisher=Пучина (Puchina) |location=Moscow and Leningrad (St. Petersburg), Russia |language=ru}}

• English translation: {{cite book |last1=Kozo-Polyansky |first1=Boris Mikhaylovich |translator-last=Fet |translator-first=Victor |editor-last=Margulis |editor-first=Lynn |title=Symbiogenesis: A New Principle of Evolution |date=2010 |publisher=Harvard University Press |location=Cambridge, Massachusetts |ref=none}}
• Reviewed in: {{cite journal |last1=Niklas |first1=Karl J. |title=Boris M. Kozo-Polyansky, Symbiogenesis: A New Principle of Evolution |journal=Symbiosis |date=2010 |volume=52 |issue=1 |pages=49–50 |doi=10.1007/s13199-010-0098-7|bibcode=2010Symbi..52...49N |s2cid=41635248 |ref=none}} he wrote, "The theory of symbiogenesis is a theory of selection relying on the phenomenon of symbiosis."{{cite book |last1=Corning |first1=Peter A. |title=Holistic Darwinism: Synergy, Cybernetics, and the Bioeconomics of Evolution |year=2010 |publisher=University of Chicago Press |location=Chicago |isbn=978-0-22611-633-4 |page=81 |url=https://books.google.com/books?id=NDeW4UNRmkwC}}

These theories did not gain traction until more detailed electron-microscopic comparisons between cyanobacteria and chloroplasts were made, such as by Hans Ris in 1961 and 1962.{{cite journal |last1=Ris |first1=Hans |last2=Plaut |first2=Walter |title=Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas |journal=The Journal of Cell Biology |volume=13 |issue=3 |pages=383–91 |date=June 1962 |pmid=14492436 |pmc=2106071 |doi=10.1083/jcb.13.3.383 }}{{cite journal |last1=Ris |first1=Hans |last2=Singh |first2=R. N. |title=Electron microscope studies on blue-green algae |journal=The Journal of Biophysical and Biochemical Cytology |volume=9 |issue=1 |pages=63–80 |date=January 1961 |pmid=13741827 |pmc=2224983 |doi=10.1083/jcb.9.1.63 }} These, combined with the discovery that plastids and mitochondria contain their own DNA,{{cite journal |last1=Stocking |first1=C. |last2=Gifford |first2=E. |title=Incorporation of thymidine into chloroplasts of Spirogyra |journal=Biochem. Biophys. Res. Commun. |year=1959 |volume=1 |issue=3 |pages =159–64 |doi=10.1016/0006-291X(59)90010-5}} led to a resurrection of the idea of symbiogenesis in the 1960s.

Lynn Margulis advanced and substantiated the theory with microbiological evidence in a 1967 paper, On the origin of mitosing cells.{{cite journal |last=Sagan |first=Lynn |title=On the origin of mitosing cells |journal=Journal of Theoretical Biology |volume=14 |issue=3 |pages=255–74 |date=March 1967 |pmid=11541392 |doi=10.1016/0022-5193(67)90079-3 |bibcode=1967JThBi..14..225S |author-link=Lynn Margulis }} In her 1981 work Symbiosis in Cell Evolution she argued that eukaryotic cells originated as communities of interacting entities, including endosymbiotic spirochaetes that developed into eukaryotic flagella and cilia. This last idea has not received much acceptance, because flagella lack DNA and do not show ultrastructural similarities to bacteria or to archaea (see also: Evolution of flagella and Prokaryotic cytoskeleton). According to Margulis and Dorion Sagan,{{cite book |last1=Margulis |first1=Lynn |author-link=Lynn Margulis |last2=Sagan |first2=Dorion |author2-link=Dorion Sagan |title=Microcosmos: Four Billion Years of Microbial Evolution |year=1997 |publisher=University of California Press |location=Berkeley, Los Angeles, London |isbn=0-520-21064-6 |page=29 |url=https://books.google.com/books?id=eo_sMMRxgAUC}} "Life did not take over the globe by combat, but by networking" (i.e., by cooperation). Christian de Duve proposed that the peroxisomes may have been the first endosymbionts, allowing cells to withstand growing amounts of free molecular oxygen in the Earth's atmosphere. However, it now appears that peroxisomes may be formed de novo, contradicting the idea that they have a symbiotic origin.{{cite journal |last1=Gabaldón |first1=Toni |last2=Snel |first2=Berend |last3=Zimmeren |first3=Frank van |last4=Hemrika |first4=Wieger |last5=Tabak |first5=Henk |last6=Huynen |first6=Martijn A. |display-authors=3 |title=Origin and evolution of the peroxisomal proteome |journal=Biology Direct |volume=1 |issue=1 |date=23 March 2006 |page=8 |doi=10.1186/1745-6150-1-8 |pmid=16556314 |pmc=1472686 |doi-access=free }}

(Provides evidence that contradicts an endosymbiotic origin of peroxisomes, and suggests instead that they originate evolutionarily from the endoplasmic reticulum) The fundamental theory of symbiogenesis as the origin of mitochondria and chloroplasts is now widely accepted.{{Cite journal |last=Cornish-Bowden |first=Athel |title=Lynn Margulis and the origin of the eukaryotes |journal=Journal of Theoretical Biology |series=The origin of mitosing cells: 50th anniversary of a classic paper by Lynn Sagan (Margulis) |date=7 December 2017 |volume=434 |page=1 |doi=10.1016/j.jtbi.2017.09.027 |pmid=28992902 |bibcode=2017JThBi.434....1C |url=https://www.sciencedirect.com/science/article/pii/S0022519317304459 |url-access=subscription }}

Symbiogenesis revolutionized the history of evolution by proposing a mechanism for evolutionary development not encompassed in the original Darwininan vision. Symbiogenesis demonstrated that major evolutionary advancements, particularly the origin of eukaryotic cells, may have resulted from symbiotic mergers rather than from gradual mutations and individual competition, i.e., classical natural selection. Accordingly, symbiogenic theory suggests that endosymbiosis may be a powerful force in generating evolutionary novelty, beyond that which can be explained by natural selection alone.{{Cite journal |last=O'Malley |first=Maureen A. |date=2015-08-18 |title=Endosymbiosis and its implications for evolutionary theory |journal=Proceedings of the National Academy of Sciences |volume=112 |issue=33 |pages=10270–10277 |doi=10.1073/pnas.1421389112 |doi-access=free |pmc=4547300 |pmid=25883268}}

File:Serial endosymbiosis.svg of the origin of eukaryotic cells. Evidence now shows that a mitochondrion-less eukaryote has never existed, i.e. the nucleus was acquired at the same time as the mitochondria.{{cite journal | vauthors = Pisani D, Cotton JA, McInerney JO | title = Supertrees disentangle the chimerical origin of eukaryotic genomes | journal = Molecular Biology and Evolution | volume = 24 | issue = 8 | pages = 1752–1760 | date = August 2007 | pmid = 17504772 | doi = 10.1093/molbev/msm095 | doi-access = free }}]]

Biologists usually distinguish organelles from endosymbionts – whole organisms living inside other organisms – by their reduced genome sizes.{{cite journal |last1=Keeling |first1=P. J. |last2=Archibald |first2=J. M. |title=Organelle evolution: what's in a name? |journal=Current Biology |volume=18 |issue=8 |pages=R345-7 |date=April 2008 |pmid=18430636 |doi=10.1016/j.cub.2008.02.065 |s2cid=11520942 |doi-access=free |bibcode=2008CBio...18.R345K }} As an endosymbiont evolves into an organelle, most of its genes are transferred to the host cell genome.{{cite book |last1=Syvanen |first1=Michael |last2=Kado |first2=Clarence I. |title=Horizontal Gene Transfer |date=30 January 2002 |publisher=Academic Press |page=405 |isbn=978-0126801262}} The host cell and organelle therefore need to develop a transport mechanism that enables the return of the protein products needed by the organelle but now manufactured by the cell.

Alphaproteobacteria were formerly thought to be the free-living organisms most closely related to mitochondria.{{cite journal |last1=Timmis |first1=Jeremy N. |last2=Ayliffe |first2=Michael A. |last3=Huang |first3=Chun Y. |last4=Martin |first4=William |author4-link=William F. Martin |title=Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes |journal=Nature Reviews Genetics |volume=5 |issue=2 |year=2004 |doi=10.1038/nrg1271 |pages=123–135|pmid=14735123 |s2cid=2385111 }} Later research indicates that mitochondria are most closely related to Pelagibacterales bacteria, in particular, those in the SAR11 clade.{{cite web |url=https://www.sciencedaily.com/releases/2011/07/110725190046.htm |title=Mitochondria Share an Ancestor With SAR11, a Globally Significant Marine Microbe |date=July 25, 2011 |website=ScienceDaily |access-date=26 July 2011}}{{cite journal |last1=Thrash |first1=J. Cameron |last2=Boyd |first2=Alex |last3=Huggett |first3=Megan J. |last4=Grote |first4=Jana |last5=Carini |first5=Paul |last6=Yoder |first6=Ryan J. |last7=Robbertse |first7=Barbara |last8=Spatafora |first8=Joseph W. |last9=Rappé |first9=Michael S. |last10=Giovannoni |first10=Stephen J. |display-authors=3 |title=Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade |journal=Scientific Reports |volume=1 |issue=1 |date=14 June 2011 |page=13 |doi=10.1038/srep00013 |pmid=22355532 |pmc=3216501 |bibcode=2011NatSR...1...13T }}

Nitrogen-fixing filamentous cyanobacteria are the free-living organisms most closely related to plastids.{{cite journal |last1=Deusch |first1=O. |last2=Landan |first2=G. |last3=Roettger |first3=M. |last4=Gruenheit |first4=N. |last5=Kowallik |first5=K. V. |last6=Allen |first6=J. F. |last7=Martin |first7=W. |last8=Dagan |first8=T. |display-authors=3 |title=Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a Heterocyst-Forming Plastid Ancestor |journal=Molecular Biology and Evolution |volume=25 |issue=4 |date=14 February 2008 |doi=10.1093/molbev/msn022 |pages=748–761|pmid=18222943 }}{{cite journal |last1=Ochoa de Alda |first1=Jesús A. G. |last2=Esteban |first2=Rocío |last3=Diago |first3=María Luz |last4=Houmard |first4=Jean |display-authors=3 |title=The plastid ancestor originated among one of the major cyanobacterial lineages |journal=Nature Communications |volume=5 |issue=1 |date=15 September 2014 |page=4937 |doi=10.1038/ncomms5937 |pmid=25222494 |bibcode=2014NatCo...5.4937O |doi-access=free }}

Both cyanobacteria and alphaproteobacteria maintain a large (>6{{nbsp}}Mb) genome encoding thousands of proteins. Plastids and mitochondria exhibit a dramatic reduction in genome size when compared with their bacterial relatives. Chloroplast genomes in photosynthetic organisms are normally 120–200{{nbsp}}kb{{cite journal |last1=Lila Koumandou |first1=V. |last2=Nisbet |first2=R. Ellen R. |last3=Barbrook |first3=Adrian C. |last4=Howe |first4=Christopher J. |display-authors=3 |title=Dinoflagellate chloroplasts—where have all the genes gone? |journal=Trends in Genetics |volume=20 |issue=5 |pages=261–267 |date=May 2004 |pmid=15109781 |doi=10.1016/j.tig.2004.03.008 }} encoding 20–200 proteins and mitochondrial genomes in humans are approximately 16{{nbsp}}kb and encode 37 genes, 13 of which are proteins.{{cite journal |last=Taanman |first=J. W. |title=The mitochondrial genome: structure, transcription, translation and replication |journal=Biochimica et Biophysica Acta (BBA) - Bioenergetics |volume=1410 |issue=2 |pages=103–23 |date=February 1999 |pmid=10076021 |doi=10.1016/S0005-2728(98)00161-3 |doi-access=free }} Using the example of the freshwater amoeboid, however, Paulinella chromatophora, which contains chromatophores found to be evolved from cyanobacteria, Keeling and Archibald argue that this is not the only possible criterion; another is that the host cell has assumed control of the regulation of the former endosymbiont's division, thereby synchronizing it with the cell's own division. Nowack and her colleagues gene sequenced the chromatophore (1.02{{nbsp}}Mb) and found that only 867 proteins were encoded by these photosynthetic cells. Comparisons with their closest free living cyanobacteria of the genus Synechococcus (having a genome size 3{{nbsp}}Mb, with 3300 genes) revealed that chromatophores had undergone a drastic genome shrinkage. Chromatophores contained genes that were accountable for photosynthesis but were deficient in genes that could carry out other biosynthetic functions; this observation suggests that these endosymbiotic cells are highly dependent on their hosts for their survival and growth mechanisms. Thus, these chromatophores were found to be non-functional for organelle-specific purposes when compared with mitochondria and plastids. This distinction could have promoted the early evolution of photosynthetic organelles.{{cite journal |last1=Nowack |first1=E. C. |last2=Melkonian |first2=M. |last3=Glockner |first3=G. |title=Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes |journal=Current Biology |volume=18 |issue=6 |pages=410–8 |date=March 2008 |pmid=18356055 |doi=10.1016/j.cub.2008.02.051 |s2cid=15929741 |doi-access=free |bibcode=2008CBio...18..410N }}

The loss of genetic autonomy, that is, the loss of many genes from endosymbionts, occurred very early in evolutionary time.{{cite journal |last1=Barbrook |first1=Adrian C. |last2=Howe |first2=Christopher J. |last3=Purton |first3=Saul |title=Why are plastid genomes retained in non-photosynthetic organisms? |journal=Trends in Plant Science |volume=11 |issue=2 |pages=101–8 |date=February 2006 |pmid=16406301 |doi=10.1016/j.tplants.2005.12.004 }} Taking into account the entire original endosymbiont genome, there are three main possible fates for genes over evolutionary time. The first is the loss of functionally redundant genes, in which genes that are already represented in the nucleus are eventually lost. The second is the transfer of genes to the nucleus, while the third is that genes remain in the organelle that was once an organism.{{cite journal |last=Leister |first=D. |title=Origin, evolution and genetic effects of nuclear insertions of organelle DNA |journal=Trends in Genetics |volume=21 |issue=12 |pages=655–63 |date=December 2005 |pmid=16216380 |doi=10.1016/j.tig.2005.09.004 |url=http://edoc.mpg.de/277780 |hdl=11858/00-001M-0000-0012-3B56-7 |hdl-access=free }}{{cite journal |last=Keeling |first=P. J. |title=Diversity and evolutionary history of plastids and their hosts |journal=American Journal of Botany |volume=91 |issue=10 |pages=1481–93 |date=October 2004 |pmid=21652304 |doi=10.3732/ajb.91.10.1481 |doi-access=free }}{{cite journal |last=Archibald |first=J. M. |title=The puzzle of plastid evolution |journal=Current Biology |volume=19 |issue=2 |pages=R81–R88 |date=January 2009 |pmid=19174147 |doi=10.1016/j.cub.2008.11.067 |s2cid=51989 |doi-access=free |bibcode=2009CBio...19..R81A }} The loss of autonomy and integration of the endosymbiont with its host can be primarily attributed to nuclear gene transfer. As organelle genomes have been greatly reduced over evolutionary time, nuclear genes have expanded and become more complex. As a result, many plastid and mitochondrial processes are driven by nuclear encoded gene products. In addition, many nuclear genes originating from endosymbionts have acquired novel functions unrelated to their organelles.

The mechanisms of gene transfer are not fully known; however, multiple hypotheses exist to explain this phenomenon. The possible mechanisms include the Complementary DNA (cDNA) hypothesis and the bulk flow hypothesis.

The cDNA hypothesis involves the use of messenger RNA (mRNAs) to transport genes from organelles to the nucleus where they are converted to cDNA and incorporated into the genome. The cDNA hypothesis is based on studies of the genomes of flowering plants. Protein coding RNAs in mitochondria are spliced and edited using organelle-specific splice and editing sites. Nuclear copies of some mitochondrial genes, however, do not contain organelle-specific splice sites, suggesting a processed mRNA intermediate. The cDNA hypothesis has since been revised as edited mitochondrial cDNAs are unlikely to recombine with the nuclear genome and are more likely to recombine with their native mitochondrial genome. If the edited mitochondrial sequence recombines with the mitochondrial genome, mitochondrial splice sites would no longer exist in the mitochondrial genome. Any subsequent nuclear gene transfer would therefore also lack mitochondrial splice sites.

The bulk flow hypothesis is the alternative to the cDNA hypothesis, stating that escaped DNA, rather than mRNA, is the mechanism of gene transfer. According to this hypothesis, disturbances to organelles, including autophagy (normal cell destruction), gametogenesis (the formation of gametes), and cell stress release DNA which is imported into the nucleus and incorporated into the nuclear DNA using non-homologous end joining (repair of double stranded breaks). For example, in the initial stages of endosymbiosis, due to a lack of major gene transfer, the host cell had little to no control over the endosymbiont. The endosymbiont underwent cell division independently of the host cell, resulting in many "copies" of the endosymbiont within the host cell. Some of the endosymbionts lysed (burst), and high levels of DNA were incorporated into the nucleus. A similar mechanism is thought to occur in tobacco plants, which show a high rate of gene transfer and whose cells contain multiple chloroplasts. In addition, the bulk flow hypothesis is also supported by the presence of non-random clusters of organelle genes, suggesting the simultaneous movement of multiple genes.

Ford Doolittle proposed that (whatever the mechanism) gene transfer behaves like a ratchet, resulting in unidirectional transfer of genes from the organelle to the nuclear genome.{{Cite journal |last=Ford Doolittle |first=W |date=1998-12-01 |title=You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes |url=https://www.sciencedirect.com/science/article/pii/S0168952598014942 |journal=Trends in Genetics |volume=14 |issue=8 |pages=307–311 |doi=10.1016/S0168-9525(98)01494-2 |pmid=9724962 |issn=0168-9525|url-access=subscription }} When genetic material from an organelle is incorporated into the nuclear genome, either the organelle or nuclear copy of the gene may be lost from the population. If the organelle copy is lost and this is fixed, or lost through genetic drift, a gene is successfully transferred to the nucleus. If the nuclear copy is lost, horizontal gene transfer can occur again, and the cell can 'try again' to have successful transfer of genes to the nucleus. In this ratchet-like way, genes from an organelle would be expected to accumulate in the nuclear genome over evolutionary time.

{{further|Eukaryogenesis}}

Endosymbiotic theory for the origin of mitochondria suggests that the proto-eukaryote engulfed a protomitochondrion, and this endosymbiont became an organelle, a major step in eukaryogenesis, the creation of the eukaryotes.{{cite journal |last1=Zimorski |first1=Verena |last2=Ku |first2=Chuan |last3=Martin |first3=William F |last4=Gould |first4=Sven B |title=Endosymbiotic theory for organelle origins |journal=Current Opinion in Microbiology |volume=22 |year=2014 |doi=10.1016/j.mib.2014.09.008 |pages=38–48|pmid=25306530 }}

File:Mitochondria, mammalian lung - TEM.jpg: mitochondrion has a matrix and membranes, like a free-living alphaproteobacterial cell, from which it may derive.]]

Mitochondria are organelles that synthesize the energy-carrying molecule ATP for the cell by metabolizing carbon-based macromolecules.{{Cite web |url=https://www.nature.com/scitable/topicpage/mitochondria-14053590 |title=Mitochondria, Cell Energy, ATP Synthase: Learn Science at Scitable |website=www.nature.com |access-date=24 March 2019}} The presence of DNA in mitochondria and proteins, derived from mtDNA, suggest that this organelle may have been a prokaryote prior to its integration into the proto-eukaryote.{{cite journal |last=Gruber |first=A. |title=What's in a name? How organelles of endosymbiotic origin can be distinguished from endosymbionts |journal=Microbial Cell |volume=6 |issue=2 |pages=123–133 |date=January 2019 |pmid=30740457 |pmc=6364258 |doi=10.15698/mic2019.02.668 }} Mitochondria are regarded as organelles rather than endosymbionts because mitochondria and the host cells share some parts of their genome, undergo division simultaneously, and provide each other with means to produce energy. The endomembrane system and nuclear membrane were hypothesized to have derived from the protomitochondria.{{cite journal |last1=Gould |first1=Sven B. |last2=Garg |first2=Sriram G. |last3=Martin |first3=William F. |title=Bacterial Vesicle Secretion and the Evolutionary Origin of the Eukaryotic Endomembrane System |journal=Trends in Microbiology |volume=24 |issue=7 |pages=525–534 |date=July 2016 |pmid=27040918 |doi=10.1016/j.tim.2016.03.005 }}{{cite journal |last1=Martin |first1=William F.|last2=Garg |first2=Sriram |last3=Zimorski |first3=Verena |title=Endosymbiotic theories for eukaryote origin |journal=Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences |volume=370 |issue=1678 |pages=20140330 |date=September 2015 |pmid=26323761 |pmc=4571569 |doi=10.1098/rstb.2014.0330 }}{{cite journal |last1=Garavís |first1=Miguel |last2=González |first2=Carlos |last3=Villasante |first3=Alfredo |title=On the origin of the eukaryotic chromosome: the role of noncanonical DNA structures in telomere evolution |journal=Genome Biology and Evolution |volume=5 |issue=6 |pages=1142–50 |date=June 2013 |pmid=23699225 |pmc=3698924 |doi=10.1093/gbe/evt079 }}

The presence of a nucleus is one major difference between eukaryotes and prokaryotes.{{Cite web |url=https://www.nature.com/scitable/content/typical-prokaryotic-left-and-eukaryotic-right-cells-14665031 |title=Typical prokaryotic (left) and eukaryotic (right) cells: Learn Science at Scitable |website=www.nature.com |access-date=2019-03-24}} Some conserved nuclear proteins between eukaryotes and prokaryotes suggest that these two types had a common ancestor.{{cite journal |last1=Devos |first1=Damien P. |last2=Gräf |first2=Ralph |last3=Field |first3=Mark C. |title=Evolution of the nucleus |journal=Current Opinion in Cell Biology |volume=28 |pages=8–15 |date=June 2014 |issue=100 |pmid=24508984 |pmc=4071446 |doi=10.1016/j.ceb.2014.01.004 }} Another theory behind nucleation is that early nuclear membrane proteins caused the cell membrane to fold and form a sphere with pores like the nuclear envelope.{{cite journal |last1=Wilson |first1=Katherine L. |last2=Dawson |first2=Scott C. |title=Evolution: functional evolution of nuclear structure |journal=Journal of Cell Biology |volume=195 |issue=2 |pages=171–81 |date=October 2011 |pmid=22006947 |pmc=3198171 |doi=10.1083/jcb.201103171 }}

As a way of forming a nuclear membrane, endosymbiosis could be expected to use less energy than if the cell was to develop a metabolic process to fold the cell membrane for the purpose. Digesting engulfed cells without energy-producing mitochondria would have been challenging for the host cell. On this view, membrane-bound bubbles or vesicles leaving the protomitochondria may have formed the nuclear envelope.

The process of symbiogenesis by which the early eukaryotic cell integrated the proto-mitochondrion likely included protection of the archaeal host genome from the release of reactive oxygen species. These would have been formed during oxidative phosphorylation and ATP production by the proto-mitochondrion. The nuclear membrane may have evolved as an adaptive innovation for protecting against nuclear genome DNA damage caused by reactive oxygen species.{{cite book |last1=Bernstein |first1=H. |last2=Bernstein |first2=C. |chapter=Sexual communication in archaea, the precursor to meiosis |pages=103–117 |title=Biocommunication of Archaea |editor=Witzany, G. |date=2017 |publisher=Springer International Publishing |isbn=978-3-319-65535-2 |doi=10.1007/978-3-319-65536-9 |s2cid=26593032 }} Substantial transfer of genes from the ancestral proto-mitochondrial genome to the nuclear genome likely occurred during early eukaryotic evolution.{{cite journal |last1=Gabaldón |first1=T. |last2=Huynen |first2=M. A. |title=Reconstruction of the proto-mitochondrial metabolism |journal=Science |volume=301 |issue=5633 |pages=609 |date=August 2003 |pmid=12893934 |doi=10.1126/science.1085463 |s2cid=28868747 }} The greater protection of the nuclear genome against reactive oxygen species afforded by the nuclear membrane may explain the adaptive benefit of this gene transfer.

File:Endomembrane system diagram en.svg

Modern eukaryotic cells use the endomembrane system to transport products and wastes in, within, and out of cells. The membrane of nuclear envelope and endomembrane vesicles are composed of similar membrane proteins.{{cite journal |last1=Liashkovich |first1=Ivan |last2=Shahin |first2=Victor |title=Functional implication of the common evolutionary origin of nuclear pore complex and endomembrane management systems |journal=Seminars in Cell and Developmental Biology |volume=68 |pages=10–17 |date=August 2017 |pmid=28473267 |doi=10.1016/j.semcdb.2017.04.006 }} These vesicles also share similar membrane proteins with the organelle they originated from or are traveling towards. This suggests that what formed the nuclear membrane also formed the endomembrane system. Prokaryotes do not have a complex internal membrane network like eukaryotes, but they could produce extracellular vesicles from their outer membrane. After the early prokaryote was consumed by a proto-eukaryote, the prokaryote would have continued to produce vesicles that accumulated within the cell. Interaction of internal components of vesicles may have led to the endoplasmic reticulum and the Golgi apparatus, both being parts of the endomembrane system.

The syntrophy hypothesis, proposed by López-García and Moreira around the year 2000, suggested that eukaryotes arose by combining the metabolic capabilities of an archaean, a fermenting deltaproteobacterium, and a methanotrophic alphaproteobacterium which became the mitochondrion. In 2020, the same team updated their syntrophy proposal to cover an promethearchaeon that produced hydrogen with deltaproteobacterium that oxidised sulphur. A third organism, an alphaproteobacterium able to respire both aerobically and anaerobically, and to oxidise sulphur, developed into the mitochondrion; it may possibly also have been able to photosynthesise.{{cite journal | last1=López-García | first1=Purificación | last2=Moreira | first2=David | title=The Syntrophy hypothesis for the origin of eukaryotes revisited | journal=Nature Microbiology | volume=5 | issue=5 | date=2020-04-27 | issn=2058-5276 | doi=10.1038/s41564-020-0710-4 | pages=655–667| pmid=32341569 | s2cid=81678433 | url=https://hal.archives-ouvertes.fr/hal-02988531/file/Final_submitted_ms.pdf }}

The question of when the transition from prokaryotic to eukaryotic form occurred and when the first crown group eukaryotes appeared on earth is unresolved. The oldest known body fossils that can be positively assigned to the Eukaryota are acanthomorphic acritarchs from the 1.631 Gya Deonar Formation of India.{{Cite journal |last=Prasad |first=Pijai |date=August 2005 |title=Organic-walled microfossils from the Proterozoic Vindhyan Supergroup of Son Valley, Madhya Pradesh, India |url=http://14.139.63.228:8080/pbrep/bitstream/123456789/1084/1/PbV54_13.pdf |journal=Paleobotanist |volume=54 }} These fossils can still be identified as derived post-nuclear eukaryotes with a sophisticated, morphology-generating cytoskeleton sustained by mitochondria.{{Cite journal |last=Butterfield |first=Nicholas J. |date=2014-11-26 |title=Early evolution of the Eukaryota |journal=Palaeontology |volume=58 |issue=1 |pages=5–17 |doi=10.1111/pala.12139|doi-access=free }} This fossil evidence indicates that endosymbiotic acquisition of alphaproteobacteria must have occurred before 1.6 Gya. Molecular clocks have also been used to estimate the last eukaryotic common ancestor, however these methods have large inherent uncertainty and give a wide range of dates. Reasonable results include the estimate of c. 1.8 Gya.{{cite journal |last1=Parfrey |first1=Laura Wegener |last2=Lahr |first2=Daniel J. G. |last3=Knoll |first3=Andrew H. |last4=Katz |first4=Laura A. |title=Estimating the timing of early eukaryotic diversification with multigene molecular clocks |journal=Proceedings of the National Academy of Sciences of the United States of America |volume=108 |issue=33 |pages=13624–9 |date=August 2011 |pmid=21810989 |pmc=3158185 |doi=10.1073/pnas.1110633108 |bibcode=2011PNAS..10813624P |doi-access=free }} A 2.3 Gya estimate{{cite journal |last1=Hedges |first1=S. Blair |last2=Blair |first2=Jaime E. |last3=Venturi |first3=Maria L. |last4=Shoe |first4=Jason L. |title=A molecular timescale of eukaryote evolution and the rise of complex multicellular life |journal=BMC Evolutionary Biology |volume=4 |pages=2 |date=January 2004 |pmid=15005799 |pmc=341452 |doi=10.1186/1471-2148-4-2 |doi-access=free }} also seems reasonable, and has the added attraction of coinciding with one of the most pronounced biogeochemical perturbations in Earth history, the early Palaeoproterozoic Great Oxygenation Event. The marked increase in atmospheric oxygen concentrations at that time has been suggested as a contributing cause of eukaryogenesis, inducing the evolution of oxygen-detoxifying mitochondria.{{cite journal |last1=Gross |first1=Jeferson |last2=Bhattacharya |first2=Debashish |title=Uniting sex and eukaryote origins in an emerging oxygenic world |journal=Biology Direct |volume=5 |pages=53 |date=August 2010 |pmid=20731852 |pmc=2933680 |doi=10.1186/1745-6150-5-53 |doi-access=free }} Alternatively, the Great Oxidation Event might be a consequence of eukaryogenesis, and its impact on the export and burial of organic carbon.{{Cite journal |last=Butterfield |first=Nicholas J. |date=1997 |title=Plankton ecology and the Proterozoic-Phanerozoic transition |journal=Paleobiology |volume=23 |issue=2 |pages=247–262 |doi=10.1017/S009483730001681X|bibcode=1997Pbio...23..247B |s2cid=140642074 }}

File:Map of the human mitochondrial genome.svg has retained genes encoding 2 rRNAs (blue), 22 tRNAs (white), and 13 redox proteins (yellow, orange, red).]]

Some endosymbiont genes remain in the organelles. Plastids and mitochondria retain genes encoding rRNAs, tRNAs, proteins involved in redox reactions, and proteins required for transcription, translation, and replication. There are many hypotheses to explain why organelles retain a small portion of their genome; however no one hypothesis will apply to all organisms, and the topic is still quite controversial. The hydrophobicity hypothesis states that highly hydrophobic (water hating) proteins (such as the membrane bound proteins involved in redox reactions) are not easily transported through the cytosol and therefore these proteins must be encoded in their respective organelles. The code disparity hypothesis states that the limit on transfer is due to differing genetic codes and RNA editing between the organelle and the nucleus. The redox control hypothesis states that genes encoding redox reaction proteins are retained in order to effectively couple the need for repair and the synthesis of these proteins. For example, if one of the photosystems is lost from the plastid, the intermediate electron carriers may lose or gain too many electrons, signalling the need for repair of a photosystem. The time delay involved in signalling the nucleus and transporting a cytosolic protein to the organelle results in the production of damaging reactive oxygen species. The final hypothesis states that the assembly of membrane proteins, particularly those involved in redox reactions, requires coordinated synthesis and assembly of subunits; however, translation and protein transport coordination is more difficult to control in the cytoplasm.{{Cite journal |last1=Giannakis |first1=Konstantinos |last2=Arrowsmith |first2=Samuel J. |last3=Richards |first3=Luke |last4=Gasparini |first4=Sara |last5=Chustecki |first5=Joanna M. |last6=Røyrvik |first6=Ellen C. |last7=Johnston |first7=Iain G. |display-authors=3 |date=16 September 2022 |title=Evolutionary inference across eukaryotes identifies universal features shaping organelle gene retention |journal=Cell Systems |volume=13 |issue=11 |pages=874–884.e5 |doi=10.1016/j.cels.2022.08.007 |pmid=36115336|s2cid=252337501 |doi-access=free |hdl=11250/3045694 |hdl-access=free }}

The majority of the genes in the mitochondria and plastids are related to the expression (transcription, translation and replication) of genes encoding proteins involved in either photosynthesis (in plastids) or cellular respiration (in mitochondria). One might predict that the loss of photosynthesis or cellular respiration would allow for the complete loss of the plastid genome or the mitochondrial genome respectively. While there are numerous examples of mitochondrial descendants (mitosomes and hydrogenosomes) that have lost their entire organellar genome,{{cite journal |last=Howe |first=Christopher J. |title=Cellular evolution: what's in a mitochondrion? |journal=Current Biology |volume=18 |issue=10 |pages=R429–R431 |date=May 2008 |pmid=18492476 |doi=10.1016/j.cub.2008.04.007 |s2cid=15730462 |doi-access=free |bibcode=2008CBio...18.R429H }} non-photosynthetic plastids tend to retain a small genome. There are two main hypotheses to explain this occurrence:

The essential tRNA hypothesis notes that there have been no documented functional plastid-to-nucleus gene transfers of genes encoding RNA products (tRNAs and rRNAs). As a result, plastids must make their own functional RNAs or import nuclear counterparts. The genes encoding tRNA-Glu and tRNA-fmet, however, appear to be indispensable. The plastid is responsible for haem biosynthesis, which requires plastid encoded tRNA-Glu (from the gene trnE) as a precursor molecule. Like other genes encoding RNAs, trnE cannot be transferred to the nucleus. In addition, it is unlikely trnE could be replaced by a cytosolic tRNA-Glu as trnE is highly conserved; single base changes in trnE have resulted in the loss of haem synthesis. The gene for tRNA-formylmethionine (tRNA-fmet) is also encoded in the plastid genome and is required for translation initiation in both plastids and mitochondria. A plastid is required to continue expressing the gene for tRNA-fmet so long as the mitochondrion is translating proteins.

The limited window hypothesis offers a more general explanation for the retention of genes in non-photosynthetic plastids.{{cite journal |last=Lane |first=Nick |author-link=Nick Lane |title=Plastids, genomes, and the probability of gene transfer |journal=Genome Biology and Evolution |volume=3 |pages=372–374 |date=2011 |pmid=21292628 |pmc=3101016 |doi=10.1093/gbe/evr003 }} According to this hypothesis, genes are transferred to the nucleus following the disturbance of organelles. Disturbance was common in the early stages of endosymbiosis, however, once the host cell gained control of organelle division, eukaryotes could evolve to have only one plastid per cell. Having only one plastid severely limits gene transfer as the lysis of the single plastid would likely result in cell death. Consistent with this hypothesis, organisms with multiple plastids show an 80-fold increase in plastid-to-nucleus gene transfer compared with organisms with single plastids.

There are many lines of evidence that mitochondria and plastids including chloroplasts arose from bacteria.Kimball, J. 2010. [http://users.rcn.com/jkimball.ma.ultranet/BiologyPages/E/Endosymbiosis.html Kimball's Biology Pages.] {{Webarchive|url=https://web.archive.org/web/20170622083131/http://users.rcn.com/jkimball.ma.ultranet/BiologyPages/E/Endosymbiosis.html|date=2017-06-22}} Accessed October 13, 2010. An online open source biology text by Harvard professor, and author of a general biology text, John W. Kimball.Reece, J., Lisa A. Urry, Michael L. Cain, Steven A. Wasserman, Peter V. Minorsky, Robert B. Jackson, 2010. Campbell Biology. 9th Edition Benjamin Cummings; 9th Ed. (October 7, 2010){{cite book |last1=Raven |first1=P. |first2=George |last2=Johnson |first3=Kenneth |last3=Mason |first4=Jonathan |last4=Losos |first5=Susan |last5=Singer |display-authors=3 |title=Biology |publisher=McGraw-Hill |edition=9th |date=January 14, 2010 }}{{cite book |last1=Gray |first1=M. W. |year=1992 |title=The Endosymbiont Hypothesis Revisited |series=International Review of Cytology |volume=141 |pages=233–357 |doi=10.1016/S0074-7696(08)62068-9 |pmid=1452433 |isbn=9780123645449 }}{{cite journal |last1=Zimorski |first1=V. |last2=Ku |first2=C. |last3=Martin |first3=W. F. |last4=Gould |first4=S. B. |title=Endosymbiotic theory for organelle origins |journal=Current Opinion in Microbiology |volume=22 |pages=38–48 |date=December 2014 |pmid=25306530 |doi=10.1016/j.mib.2014.09.008 }}

• New mitochondria and plastids are formed only through binary fission, the form of cell division used by bacteria and archaea.{{cite journal |last=Margolin |first=William |title=FtsZ and the division of prokaryotic cells and organelles |journal=Nature Reviews. Molecular Cell Biology |volume=6 |issue=11 |pages=862–71 |date=November 2005 |pmid=16227976 |pmc=4757588 |doi=10.1038/nrm1745 }}
• If a cell's mitochondria or chloroplasts are removed, the cell does not have the means to create new ones.{{cite book |last1=Wise |first1=Robert R. |last2=Hoober |first2=J. Kenneth |title=Structure and function of plastids |year=2007 |publisher=Springer |location=Berlin |isbn=9781402065705 |page=104 |url=https://books.google.com/books?id=FKeCVPbJ3asC&pg=PA104 }} In some algae, such as Euglena, the plastids can be destroyed by certain chemicals or prolonged absence of light without otherwise affecting the cell: the plastids do not regenerate.
• Transport proteins called porins are found in the outer membranes of mitochondria and chloroplasts and are also found in bacterial cell membranes.{{cite journal |last1=Fischer |first1=K. |last2=Weber |first2=A. |last3=Brink |first3=S. |last4=Arbinger |first4=B. |last5=Schünemann |first5=D. |last6=Borchert |first6=S. |last7=Heldt |first7=H. W. |last8=Popp |first8=B. |last9=Benz |first9=R. |last10=Link |first10=T. A. |display-authors=3 |title=Porins from plants. Molecular cloning and functional characterization of two new members of the porin family |journal=The Journal of Biological Chemistry |volume=269 |issue=41 |pages=25754–60 |date=October 1994 |doi=10.1016/S0021-9258(18)47312-7 |pmid=7523392 |doi-access=free }}{{cite journal |last1=Zeth |first1=K. |last2=Thein |first2=M. |title=Porins in prokaryotes and eukaryotes: common themes and variations |journal=The Biochemical Journal |volume=431 |issue=1 |pages=13–22 |date=October 2010 |pmid=20836765 |doi=10.1042/BJ20100371 |s2cid=22073622 }}{{cite journal |last1=Fairman |first1=J. W. |last2=Noinaj |first2=N. |last3=Buchanan |first3=S. K. |title=The structural biology of β-barrel membrane proteins: a summary of recent reports |journal=Current Opinion in Structural Biology |volume=21 |issue=4 |pages=523–331 |date=August 2011 |pmid=21719274 |pmc=3164749 |doi=10.1016/j.sbi.2011.05.005 }}
• A membrane lipid cardiolipin is exclusively found in the inner mitochondrial membrane and bacterial cell membranes.{{cite journal |last1=Mileykovskaya |first1=E. |last2=Dowhan |first2=W. |title=Cardiolipin membrane domains in prokaryotes and eukaryotes |journal=Biochimica et Biophysica Acta (BBA) - Biomembranes |volume=1788 |issue=10 |pages=2084–91 |date=October 2009 |pmid=19371718 |pmc=2757463 |doi=10.1016/j.bbamem.2009.04.003 }}
• Some mitochondria and some plastids contain single circular DNA molecules that are similar to the DNA of bacteria both in size and structure.{{cite journal |last1=Timmis |first1=Jeremy |last2=Ayliffe |first2=Michael |last3=Huang |first3=Chun |last4=Martin |first4=William |title=Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes |journal=Nature Reviews. Genetics |volume=5 |issue=2 |pages=123–35 |date=February 2004 |pmid=14735123 |doi=10.1038/nrg1271 |s2cid=2385111 }}
• Genome comparisons suggest a close relationship between mitochondria and Alphaproteobacteria.{{cite journal |last1=Munoz-Gomez |first1=Sergio |last2=Susko |first2=Edward |last3=Williamson |first3=Kelsey |last4=eme |first4=Laura |last5=Slamovits |first5=Claudio H. |last6=Moreira |first6=David |last7=López-García |first7=Purificación |last8=Roger |first8=Andrew J. |display-authors=3 |title=Site-and-branch-heterogeneous analyses of an expanded dataset favour mitochondria as sister to known Alphaproteobacteria |journal=Nature Ecology and Evolution |volume=6 |pages=253–62 |date=January 2022 |issue=3 |doi=10.1038/s41559-021-01638-2 |pmid=35027725 |bibcode=2022NatEE...6..253M |s2cid=245958471 }}
• Genome comparisons suggest a close relationship between plastids and cyanobacteria.{{cite journal |last1=Dagan |first1=Tal |last2=Roettger |first2=Mayo |last3=Stucken |first3=Karina |last4=Landan |first4=Giddy |last5=Koch |first5=Robin |last6=Major |first6=Peter |last7=Gould |first7=Sven B. |last8=Goremykin |first8=Vadim V. |last9=Rippka |first9=Rosmarie |last10=Tandeau de Marsac |first10=Nicole |last11=Gugger |first11=Muriel |last12=Lockhart |first12=Peter J. |last13=Allen |first13=John F. |last14=Brune |first14=Iris |last15=Maus |first15=Irena |last16=Pühler |first16=Alfred |last17=Martin |first17=William F. |display-authors=3 |title=Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids |journal=Genome Biology and Evolution |volume=5 |issue=1 |pages=31–44 |year=2013 |pmid=23221676 |pmc=3595030 |doi=10.1093/gbe/evs117 }}
• Many genes in the genomes of mitochondria and chloroplasts have been lost or transferred to the nucleus of the host cell. Consequently, the chromosomes of many eukaryotes contain genes that originated from the genomes of mitochondria and plastids.
• Mitochondria and plastids contain their own ribosomes; these are more similar to those of bacteria (70S) than those of eukaryotes.{{cite journal |last1=Manuell |first1=Andrea L. |last2=Quispe |first2=Joel |last3=Mayfield |first3=Stephen P. |title=Structure of the chloroplast ribosome: novel domains for translation regulation |journal=PLOS Biology |volume=5 |issue=8 |pages=e209 |date=August 2007 |pmid=17683199 |pmc=1939882 |doi=10.1371/journal.pbio.0050209 |doi-access=free }}
• Proteins created by mitochondria and chloroplasts use N-formylmethionine as the initiating amino acid, as do proteins created by bacteria but not proteins created by eukaryotic nuclear genes or archaea.{{cite journal |last1=Schwartz |first1=James H. |last2=Meyer |first2=Ralph |last3=Eisenstadt |first3=Jerome M. |last4=Brawerman |first4=George |title=Involvement of N-formylmethionine in initiation of protein synthesis in cell-free extracts of Euglena gracilis |journal=Journal of Molecular Biology |volume=25 |issue=3 |pages=571–4 |date=May 1967 |pmid=5340700 |doi=10.1016/0022-2836(67)90210-0 }}{{cite journal |last1=Smith |first1=A.E. |last2=Marcker |first2=K.A. |title=N-formylmethionyl transfer RNA in mitochondria from yeast and rat liver |journal=Journal of Molecular Biology |volume=38 |issue=2 |pages=241–3 |date=December 1968 |pmid=5760639 |doi=10.1016/0022-2836(68)90409-9 }}

{{plain image with caption|Chloroplast-cyanobacterium comparison.svg|Comparison of chloroplasts and cyanobacteria showing their similarities. Both chloroplasts and cyanobacteria have a double membrane, DNA, ribosomes, and chlorophyll-containing thylakoids.|650px|center|bottom|triangle|#3fad47}}

{{see also|Plastid evolution#Secondary endosymbiosis}}

Primary endosymbiosis involves the engulfment of a cell by another free living organism. Secondary endosymbiosis occurs when the product of primary endosymbiosis is itself engulfed and retained by another free living eukaryote. Secondary endosymbiosis has occurred several times and has given rise to extremely diverse groups of algae and other eukaryotes. Some organisms can take opportunistic advantage of a similar process, where they engulf an alga and use the products of its photosynthesis, but once the prey item dies (or is lost) the host returns to a free living state. Obligate secondary endosymbionts become dependent on their organelles and are unable to survive in their absence. A secondary endosymbiosis event involving an ancestral red alga and a heterotrophic eukaryote resulted in the evolution and diversification of several other photosynthetic lineages including Cryptophyta, Haptophyta, Stramenopiles (or Heterokontophyta), and Alveolata.{{cite journal |last=McFadden |first=G. I. |title=Primary and secondary endosymbiosis and the origin of plastids |journal=Journal of Phycology |year=2001 |volume=37 |issue=6 |pages=951–959 |doi=10.1046/j.1529-8817.2001.01126.x |bibcode=2001JPcgy..37..951M |s2cid=51945442 }}

A possible secondary endosymbiosis has been observed in process in the heterotrophic protist Hatena. This organism behaves like a predator until it ingests a green alga, which loses its flagella and cytoskeleton but continues to live as a symbiont. Hatena meanwhile, now a host, switches to photosynthetic nutrition, gains the ability to move towards light, and loses its feeding apparatus.{{cite journal |last1=Okamoto |first1=N. |last2=Inouye |first2=I. |title=A secondary symbiosis in progress? |journal=Science |volume=310 |issue=5746 |pages=287 |date=October 2005 |pmid=16224014 |doi=10.1126/science.1116125 |s2cid=22081618 |url=https://www.researchgate.net/publication/7542363 }}

Despite the diversity of organisms containing plastids, the morphology, biochemistry, genomic organisation, and molecular phylogeny of plastid RNAs and proteins suggest a single origin of all extant plastids – although this theory was still being debated in 2008.{{cite journal |last1=McFadden |first1=G. I. |last2=van Dooren |first2=G. G. |title=Evolution: red algal genome affirms a common origin of all plastids |journal=Current Biology |volume=14 |issue=13 |pages=R514-6 |date=July 2004 |pmid=15242632 |doi=10.1016/j.cub.2004.06.041 |s2cid=18131616 |doi-access=free |bibcode=2004CBio...14.R514M }}{{cite journal |last1=Gould |first1=Sven B. |last2=Waller |first2=Ross F. |last3=McFadden |first3=Geoffrey I. |title=Plastid evolution |journal=Annual Review of Plant Biology |volume=59 |issue=1 |pages=491–517 |year=2008 |pmid=18315522 |doi=10.1146/annurev.arplant.59.032607.092915 |bibcode=2008AnRPB..59..491G |s2cid=30458113 }}

A unicellular marine alga, Braarudosphaera bigelowii (a coccolithophore, which is a eukaryote), has been found with a cyanobacterium as an endosymbiont. The cyanobacterium forms a nitrogen-fixing structure, dubbed the nitroplast. It divides evenly when the host cell undergoes mitosis, and many of its proteins derive from the host alga, implying that the endosymbiont has proceeded far along the path towards becoming an organelle. The cyanobacterium is named Candidatus Atelocyanobacterium thalassa, and is abbreviated UCYN-A. The alga is the first eukaryote known to have the ability to fix nitrogen.{{cite journal |last=Massana |first=Ramon |date=12 April 2024 |title=The nitroplast: A nitrogen-fixing organelle |url=https://www.science.org/doi/10.1126/science.ado8571 |journal=Science |volume=384 |issue=6692 |pages=160–161 |doi=10.1126/science.ado8571 |pmid=38603513 |bibcode=2024Sci...384..160M |issn=0036-8075 |access-date=15 April 2024 |archive-date=15 April 2024 |archive-url=https://web.archive.org/web/20240415055905/https://www.science.org/doi/10.1126/science.ado8571 |url-status=live |url-access=subscription |hdl=10261/354070 |hdl-access=free }}{{cite journal |last1=Coale |first1=Tyler H. |last2=Loconte |first2=Valentina |last3=Turk-Kubo |first3=Kendra A. |last4=Vanslembrouck |first4=Bieke |last5=Mak |first5=Wing Kwan Esther |last6=Cheung |first6=Shunyan |last7=Ekman |first7=Axel |last8=Chen |first8=Jian-Hua |last9=Hagino |first9=Kyoko |last10=Takano |first10=Yoshihito |last11=Nishimura |first11=Tomohiro |last12=Adachi |first12=Masao |last13=Le Gros |first13=Mark |last14=Larabell |first14=Carolyn |last15=Zehr |first15=Jonathan P. |title=Nitrogen-fixing organelle in a marine alga |journal=Science |volume=384 |issue=6692 |date=2024-04-12 |issn=0036-8075 |doi=10.1126/science.adk1075 |pages=217–222|pmid=38603509 |bibcode=2024Sci...384..217C }}

• Angomonas deanei, a protozoan that harbours an obligate bacterial symbiont
• Hatena arenicola, a species that appears to be in the process of acquiring an endosymbiont
• Hydrogen hypothesis, the theory that mitochondria were acquired by hydrogen-dependent archaea, their endosymbionts being facultatively anaerobic bacteria
• Kleptoplasty, the sequestering of plastids from ingested algae
• Mixotricha paradoxa, which itself is a symbiont, contains numerous endosymbiotic bacteria
• Parakaryon myojinensis, a possible result of endosymbiosis independent of eukaryotes
• Parasite Eve, fiction about endosymbiosis
• Strigomonas culicis, another protozoan that harbours an obligate bacterial symbiont
• Viral eukaryogenesis, hypothesis that the cell nucleus originated from endosymbiosis

{{reflist|30em}}

{{refbegin}}

• {{cite book |last=Alberts |first=Bruce |title=Molecular Biology of the Cell |publisher=Garland Science |location=New York |year=2002 |isbn=978-0-8153-3218-3 |ref=none}} (General textbook)
• {{cite journal |last1=Brinkman |first1=Fiona S. L. |last2=Blanchard |first2=Jeffrey L. |last3=Cherkasov |first3=Artem |last4=Av-Gay |first4=Yossef |last5=Brunham |first5=Robert C. |last6=Fernandez |first6=Rachel C. |last7=Finlay |first7=B. Brett |last8=Otto |first8=Sarah P. |last9=Ouellette |first9=B. F. Francis |last10=Keeling |first10=Patrick J. |last11=Rose |first11=Ann M. |last12=Hancock |first12=Robert E.W. |last13=Jones |first13=Steven J.M. |display-authors=3 |title=Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast |journal=Genome Research |volume=12 |issue=8 |pages=1159–67 |date=August 2002 |pmid=12176923 |pmc=186644 |doi=10.1101/gr.341802 |author-link1=Fiona Brinkman |ref=none}}
• {{cite web |last1=Cohen |first1=W. E. |last2=Gardner |first2=R. S. |title=Viral Theory and Endosymbiosis |year=1959 |url=http://www.psychoneuroendocrinology.com/symbiosis.pdf |access-date=2009-08-26 |archive-url=https://web.archive.org/web/20110715130039/http://www.psychoneuroendocrinology.com/symbiosis.pdf |archive-date=2011-07-15 |url-status=dead |ref=none}} (Discusses theory of origin of eukaryotic cells by incorporating mitochondria and chloroplasts into anaerobic cells with emphasis on 'phage bacterial and putative viral mitochondrial/chloroplast interactions.)
• {{cite journal |last=Jarvis |first=P. |title=Intracellular signalling: the chloroplast talks! |journal=Current Biology |volume=11 |issue=8 |pages=R307-10 |date=April 2001 |pmid=11369220 |doi=10.1016/S0960-9822(01)00171-3 |s2cid=11753648 |doi-access=free |bibcode=2001CBio...11.R307J |ref=none}} (Recounts evidence that chloroplast-encoded proteins affect transcription of nuclear genes, as opposed to the more well-documented cases of nuclear-encoded proteins that affect mitochondria or chloroplasts.)
• {{cite journal |last1=Blanchard |first1=J. L. |last2=Lynch |first2=M. |title=Organellar genes: why do they end up in the nucleus? |journal=Trends in Genetics |volume=16 |issue=7 |pages=315–20 |date=July 2000 |pmid=10858662 |doi=10.1016/S0168-9525(00)02053-9 |ref=none}} (Discusses theories on how mitochondria and chloroplast genes are transferred into the nucleus, and also what steps a gene needs to go through in order to complete this process.)
• {{cite journal |last1=Okamoto |first1=N. |last2=Inouye |first2=I. |title=A secondary symbiosis in progress? |journal=Science |volume=310 |issue=5746 |pages=287 |date=October 2005 |pmid=16224014 |doi=10.1126/science.1116125 |s2cid=22081618 |ref=none}}
• {{cite web |last=Understanding Science Team |title=Cells within cells: An extraordinary claim with extraordinary evidence |url=http://undsci.berkeley.edu/lessons/pdfs/endosymbiosis.pdf |publisher=University of California, Berkeley |access-date=16 February 2014 |ref=none}}

{{refend}}

• [http://tolweb.org/Eukaryotes/3 Tree of Life Eukaryotes]

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