Eukaryotic organelles supposedly evolved from their bacterial ancestors because of their benefits to host cells. However, organelles are quite often retained, even when the beneficial metabolic pathway is lost, due to something other than the original beneficial function. The organellar function essential for cell survival is, in the end, the result of organellar evolution, particularly losses of redundant metabolic pathways present in both the host and endosymbiont, followed by a gradual distribution of metabolic functions between the organelle and host. Such biological division of metabolic labor leads to mutual dependence of the endosymbiont and host. Changing environmental conditions, such as the gradual shift of an organism from aerobic to anaerobic conditions or light to dark, can make the original benefit useless. Therefore, it can be challenging to deduce the original beneficial function, if there is any, underlying organellar acquisition. However, it is also possible that the organelle is retained because it simply resists being eliminated or digested untill it becomes indispensable.

Faculty of Science University of South Bohemia 37005 České Budějovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences 37005 České Budějovice Czech Republic

Zobrazit více v PubMed

Gould S.B., Waller R.F., McFadden G.I. Plastid evolution. Annu. Rev. Plant. Biol. 2008;59:491–517. doi: 10.1146/annurev.arplant.59.032607.092915. PubMed DOI

Keeling P.J. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Ann. Rev. Plant. Biol. 2013;64:583–607. doi: 10.1146/annurev-arplant-050312-120144. PubMed DOI

Archibald J.M. Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 2015;25:R911–R921. doi: 10.1016/j.cub.2015.07.055. PubMed DOI

Gruber A. What’s a name? Why organelles of endosymbiotic origin are implicitly called by their eukaryotic species name and how they can be distinguished from endosymbionts. Microb. Cell. 2019;6:123–133. doi: 10.15698/mic2019.02.668. PubMed DOI PMC

Pallen M.J. Time to recognize that mitochondria are bacteria? Trends Microbiol. 2011;19:58–61. doi: 10.1016/j.tim.2010.11.001. PubMed DOI

Oborník M. In the beginning was the word: How terminology drives our understanding of endosymbiotic organelles. Microb. Cell. 2019;6:134–141. doi: 10.15698/mic2019.02.669. PubMed DOI PMC

Oborník M. Endosymbiotic evolution of algae, secondary heterotrophy and parasitism. Biomolecules. 2019;9:266. doi: 10.3390/biom9070266. PubMed DOI PMC

Martin W., Rujan T., Richly E., Hansen A., Cornelsen S., Lins T., Leister D., Stoebe B., Hasegawa M., Penny D. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA. 2002;99:12246–12251. doi: 10.1073/pnas.182432999. PubMed DOI PMC

Timmis J.N., Ayliffe M.A., Huang C.Y., Martin W. Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 2004;5:123–135. doi: 10.1038/nrg1271. PubMed DOI

Keeling P.J., McCutcheon J.P. Endosymbiosis: The feeling is not mutual. J. Theor. Biol. 2017;434:75–79. doi: 10.1016/j.jtbi.2017.06.008. PubMed DOI PMC

Oborník M. Photoparasitism as an intermediate state in the evolution of apicomplexan parasites. Trends Parasitol. 2020;36:727–734. doi: 10.1016/j.pt.2020.06.002. PubMed DOI

Hampl V., Čepička I., Eliáš M. Was the mitochondrion necessary to start eukaryogenesis? Trends Microbiol. 2018;27:96–104. doi: 10.1016/j.tim.2018.10.005. PubMed DOI

Martin W.F., Garg S., Zimorski V. Endosymbiotic theories for eukaryote origin. Philos. Trans. R. Soc. B. 2015;370:20140330. doi: 10.1098/rstb.2014.0330. PubMed DOI PMC

Muñoz-Gómez S.A., Wideman J.G., Roger A.J., Slamovits C.H. The origin of mitochondrial cristae from alphaproteobacteria. Mol. Evol. Biol. 2017;34:943–956. doi: 10.1093/molbev/msw298. PubMed DOI

Raymond J. The role of horizontal gene transfer in photosynthesis, oxygen production, and oxygen tolerance. Methods Mol. Biol. 2009;532:323–338. PubMed

Koblížek M., Moulisová V., Muroňová M., Oborník M. Horizontal transfers of two types of puf operons among phototrophic members of the Roseobacter clade. Folia Microbiol. 2015;60:37–43. doi: 10.1007/s12223-014-0337-z. PubMed DOI

Fischer W.W., Hemp J., Johnson J.E. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet Sci. 2016;44:647–683. doi: 10.1146/annurev-earth-060313-054810. DOI

Cavalier-Smith T. Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Euk. Microbiol. 1999;46:347–366. doi: 10.1111/j.1550-7408.1999.tb04614.x. PubMed DOI

Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int. J. Syst. Evol. Microbiol. 2002;52:297–354. doi: 10.1099/00207713-52-2-297. PubMed DOI

Delaye L., Valadez-Cano C., Perez-Zamorano B. How really ancient is Paulinella chromatophora? PLoS Curr. Tree Life. 2016;8 doi: 10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b. PubMed DOI PMC

Stephens T.G., Gabr A., Calatrava V., Grossman A.R., Bhattacharya D. Why is primary endosymbiosis so rare? New Phytol. 2021;231:1693–1699. doi: 10.1111/nph.17478. PubMed DOI PMC

Kies L. Electron microscopical investigations on Paulinella chromatophora Lauterborn, a thecamoeba containing blue-green endosymbionts (cyanelles) Protoplasma. 1974;80:69–89. doi: 10.1007/BF01666352. PubMed DOI

Kies L., Kremer B.P. Function of cyanelles in the thecamoeba Paulinella chromatophora. Naturwissenschaften. 1979;66:578–579. doi: 10.1007/BF00368819. DOI

Marin B., Nowack E.C., Melkonian M. A plastid in the making: Evidence for a second primary endosymbiosis. Protist. 2005;156:425–432. doi: 10.1016/j.protis.2005.09.001. PubMed DOI

Bodył A., Stiller J.W., Mackiewicz P. Chromalveolate plastids: Direct sescent or multiple endosymbioses? Trend. Ecol. Evol. 2009;24:119–121. doi: 10.1016/j.tree.2008.11.003. PubMed DOI

Stiller J.W., Schreiber J., Yue J., Guo H., Ding Q., Huang J. The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat. Commun. 2014;5:5764. doi: 10.1038/ncomms6764. PubMed DOI PMC

Petersen J., Ludewig A.K., Michael V., Bunk B., Jarek M., Baurain D., Brinkman H. Chromera velia, endosymbioses and the rhodoplex hypothesis—plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages) Genome Biol. Evol. 2014;6:666–684. doi: 10.1093/gbe/evu043. PubMed DOI PMC

Dorrell R.G., Bowler C. Secondary plastids of stramenopiles. Adv. Bot. Res. 2017;84:57–103.

Strassert J.F.H., Irisarri I., Williams T.A., Burki F. A molecular timescale of eukaryote evolution with implications for the origin of red algal-derived plastids. Nat. Commun. 2021;12:1879. doi: 10.1038/s41467-021-22044-z. PubMed DOI PMC

Oborník M. The birth of red complex plastids: One, three, or four times? Trends Parasitol. 2018;34:923–925. doi: 10.1016/j.pt.2018.09.001. PubMed DOI

Hadariová L., Vesteg M., Hampl V., Krajčoviš J. Reductive evolution of chloroplasts in non-photosynthetic plants, algae and protists. Curr. Genet. 2018;64:365–387. doi: 10.1007/s00294-017-0761-0. PubMed DOI

Sato S., Nakamura Y., Kaneko T., Asamizu E., Tabata S. Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res. 1999;29:283–290. doi: 10.1093/dnares/6.5.283. PubMed DOI

Tajima N., Sato S., Maruyama F., Kurokawa K., Ohta H., Tabata S., Sekine K., Moriyama T., Sato N. Analysis of the complete plastid genome of the unicellular red alga Porphyridium purpureum. J. Plant Res. 2014;127:389–397. doi: 10.1007/s10265-014-0627-1. PubMed DOI

De Koning A.P., Keeling P.J. The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol. 2006;4:12. doi: 10.1186/1741-7007-4-12. PubMed DOI PMC

Smith D.R., Lee R.W. A Plastid without a Genome: Evidence from the Nonphotosynthetic Green Algal Genus Polytomella. Plant Physiol. 2014;164:1812–1819. doi: 10.1104/pp.113.233718. PubMed DOI PMC

Nowack E.C.M., Melkonian M., Glockner G. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 2008;18:410–418. doi: 10.1016/j.cub.2008.02.051. PubMed DOI

Hallick R.B., Hong L., Drager R.G., Favreau M.R., Monfort A., Orsat B., Spielmann A., Stutz E. Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res. 1993;21:3537–3544. doi: 10.1093/nar/21.15.3537. PubMed DOI PMC

Gockel G., Hachtel W. Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist. 2000;151:347–351. doi: 10.1078/S1434-4610(04)70033-4. PubMed DOI

Zhang Z., Green B.R., Cavalier-Smith T. Single gene circles in dinoflagellate chloroplast genomes. Nature. 1999;400:155–159. doi: 10.1038/22099. PubMed DOI

Gornik S.G., Cassin A.M., MacRae J.I., Ramprasad A., Rchiad Z., McConville M.J., Bacic A., McFadden G.I., Pain A., Waller R.F. Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proc. Natl. Acad. Sci. USA. 2015;112:5767–5772. doi: 10.1073/pnas.1423400112. PubMed DOI PMC

Oudot-Le Secq M.-P., Grimwood J., Shapiro H., Armbrust E.V., Bowler C., Green B.R. Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: Comparison with other plastid genomes of the red lineage. Mol. Genet. Genom. 2007;277:427–439. doi: 10.1007/s00438-006-0199-4. PubMed DOI

Janouškovec J., Horák A., Oborník M., Lukeš J., Keeling P.J. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc. Natl. Acad. Sci. USA. 2010;107:10949–10950. doi: 10.1073/pnas.1003335107. PubMed DOI PMC

Zhu G., Marchewka M.J., Keithly J.S. Cryptosoridium parvum appears to lack a plastid genome. Microbiology. 2000;146:315–321. doi: 10.1099/00221287-146-2-315. PubMed DOI

Suzuki S., Endoh R., Manabe R., Ohkuma M., Hirakawa Y. Multiple losses of photosynthesis and convergent reductive genome evolution in the colourless green algae Prototheca. Sci. Rep. 2018;8:940. doi: 10.1038/s41598-017-18378-8. PubMed DOI PMC

Khorobrykh S., Havurinne V., Mattila H., Tyystjärvi E. Oxygen and ROSS in photosynthesis. Plants. 2020;9:91. doi: 10.3390/plants9010091. PubMed DOI PMC

Füssy Z., Záhonová K., Tomčala A., Krajčovič J., Yurchenko V., Oborník M., Eliáš M. The cryptic plastid of Euglena longa defines a new type of nonphotosynthetic plastid organelle. mSphere. 2020;5:e00675-20. doi: 10.1128/mSphere.00675-20. PubMed DOI PMC

Salomaki E.D., Kolisko M. There is treasure everywhere: Reductive plastid evolution in Apicomplexa in light of their close relatives. Biomolecules. 2019;9:378. doi: 10.3390/biom9080378. PubMed DOI PMC

Waller R.F., Kořený L. Plastid complexity in dinoflagellates: A picture of gains, losses, replacements and revisions. Adv. Bot. Res. 2017;84:105–143.

Mathur V., Kolísko M., Hehenberger E., Irwin N.A.T., Leander B.S., Kristmundsson Á., Freeman M.A., Keeling P.J. Multiple independent origins of apicomplexan-like parasites. Curr. Biol. 2019;29:1–6. doi: 10.1016/j.cub.2019.07.019. PubMed DOI

Janouškovec J., Paskerova G.G., Miroliubova T.S., Mikhailov K.V., Birley T., Aleoshin V.V., Simdyanov T.G. Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles. eLife. 2019;8:e49662. doi: 10.7554/eLife.49662. PubMed DOI PMC

Toso M.A., Omoto C.K. Gregarina niphandrodes may lack both a plastid genome and organelle. J. Eukaryot. Microbiol. 2007;54:66–72. doi: 10.1111/j.1550-7408.2006.00229.x. PubMed DOI

Gray W., Burger G., Derelle R., Klimeš V., Leger M.M., Sarrasin M., Vlček Č., Roger A.J., Eliáš M., Lang B.F. The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoi, a protist with the most gene-rich and bacteria-like mitochondrial genome. BMC Biol. 2020;18:22. doi: 10.1186/s12915-020-0741-6. PubMed DOI PMC

Lang B.F., Burger G., O’Kelly C.J., Cedergren R., Golding G.B., Lemieux C., Sankoff D., Turmel M., Gray M.W. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature. 1997;387:493–497. doi: 10.1038/387493a0. PubMed DOI

Anderson S., Bankier A.T., Barrell B.G., de Bruijn M.H.L., Coulson A.R., Drouin J., Eperon I.C., Nierlich D.P., Roe B.A., Sanger F., et al. Sequence and organization of the human mitochondrial genome. Nature. 1981;290:457–465. doi: 10.1038/290457a0. PubMed DOI

Dong S., Zhao C., Chen F., Liu Y., Zhang S., Wu H., Zhang L., Liu Y. The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination. BMC Genom. 2018;19:614. doi: 10.1186/s12864-018-4991-4. PubMed DOI PMC

De Graaf R.M., Ricard G., van Alen T.A., Duarte I., Dutilh B.E., Burgtorf C., Kuiper J.W.P., van der Staay G.W.M., Tielens A.G.M., Huynen M.A., et al. The Organellar Genome and Metabolic Potential of the Hydrogen-Producing Mitochondrion of Nyctotherus ovalis. Mol. Biol. Evol. 2011;28:2379–2391. doi: 10.1093/molbev/msr059. PubMed DOI PMC

Gardner M.J., Bates P.A., Ling I.T., Moore D.J., McCready S., Gunasekera M.B.R., Wilson R.J.M., Williamson D.H. Mitochondrial DNA of the human malarial parasite Plasmodium falciparum. Mol. Biochem. Prasitol. 1988;31:11–17. doi: 10.1016/0166-6851(88)90140-5. PubMed DOI

Flegontov P., Michálek J., Janouškovec J., Lai D.H., Jirků M., Hajdušková E., Tomčala A., Otto D.T., Keeling P.J., Pain A., et al. Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites. Mol. Biol. Evol. 2015;32:1115–1131. doi: 10.1093/molbev/msv021. PubMed DOI

John U., Lu Y., Wohlrab S., Groth M., Janouškovec J., Kohli G.S., Mark F.C., Bickmeyer U., Frahat S., Felder M., et al. A aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome. Sci. Adv. 2019;5:1110. doi: 10.1126/sciadv.aav1110. PubMed DOI PMC

Roger A.J., Muñoz-Gómez S.A., Kamikawa R. The origin and diversification of mitochondria. Curr. Biol. 2017;27:R1177–R1192. doi: 10.1016/j.cub.2017.09.015. PubMed DOI

Karnkowska A., Vacek V., Zubacova Z., Treitli S.C., Petrzelková R., Eme L., Novaqk L., Zarsky V., Barlow L.D., Herman E.K. A eukaryote without a mitochondrial organelle. Curr. Biol. 2016;26:1274–1284. doi: 10.1016/j.cub.2016.03.053. PubMed DOI

Burger G., Gray M.W., Forget L., Lang B.F. Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genom. Biol. Evol. 2013;5:418–438. doi: 10.1093/gbe/evt008. PubMed DOI PMC

Oborník M., Lukeš J. The organellar genomes of Chromera and Vitrella, the phototrophic relatives of apicomplexan parasites. Ann. Rev. Microbiol. 2015;69:129–144. doi: 10.1146/annurev-micro-091014-104449. PubMed DOI

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., Martin W.F. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 2012;76:444–495. doi: 10.1128/MMBR.05024-11. PubMed DOI PMC

Calvo S.E., Mootha V.K. The mitochondrial proteome and human disease. Annu. Rev. Genom. Hum. Genet. 2010;11:25–44. doi: 10.1146/annurev-genom-082509-141720. PubMed DOI PMC

Panigrahi A.K., Ogata Y., Zíková A., Anupama A., Dalley R.A., Acestor N., Myler P.J., Stuart K.D. A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics. 2009;9:434–450. doi: 10.1002/pmic.200800477. PubMed DOI PMC

Gawryluk R.M.R., Chisholm K.A., Pinto D.M., Gray M.W. Compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa) rivals that of animals, fungi, and plants. J. Proteom. 2014;109:400–416. doi: 10.1016/j.jprot.2014.07.005. PubMed DOI

Cihlář J., Füssy Z., Horák A., Oborník M. Evolution of the tetrapyrole biosynthetic pathway in secondary algae: Conservation, redundancy and replacement. PLoS ONE. 2016;11:e0166338. doi: 10.1371/journal.pone.0166338. PubMed DOI PMC

Martin W., Müller M. The hydrogen hypothesis for the first eukaryote. Nature. 1998;392:37–41. doi: 10.1038/32096. PubMed DOI

Boxma B., de Graaf R., van der Staay G., van Alen T.A., Ricard G., Gabaldón T., van Hoek A.H.A.M., van der Staay S.Y.M., Koopman W.J.H., van Hellemond J.J., et al. An anaerobic mitochondrion that produces hydrogen. Nature. 2005;434:74–79. doi: 10.1038/nature03343. PubMed DOI

Cavalier-Smith T. Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc. Biol. Sci. 2006;273:1943–1952. doi: 10.1098/rspb.2006.3531. PubMed DOI PMC

Lyons T.W., Reinhard C.T., Planavsky N.J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature. 2014;506:307–315. doi: 10.1038/nature13068. PubMed DOI

Eme L., Sharpe S.C., Brown M.W., Roger A.J. On the age of eukaryotes: Evaluating evidence from fossils and molecular clocks. Cold Spring Harb. Perspect. Biol. 2014;6:a016139. doi: 10.1101/cshperspect.a016139. PubMed DOI PMC

Vellai T., Takacs K., Vida G. A new aspect to the origin and evolution of eukaryotes. J. Mol. Evol. 1998;46:499–507. doi: 10.1007/PL00006331. PubMed DOI

Kurland C.G., Andersson S.G. Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 2000;64:786–820. doi: 10.1128/MMBR.64.4.786-820.2000. PubMed DOI PMC

Zimorski V., Mentel M., Tielens A.G.M., Martin W.F. Energy metabolism in nanerobic eukaryotes and Earth’s late oxygenation. Free Radic. Biol. Med. 2019;140:279–294. doi: 10.1016/j.freeradbiomed.2019.03.030. PubMed DOI PMC

Imlay J.A. How oxygen damages microbes: Oxygen tolerance and obligate anaerobiosis. Adv. Microb. Physiol. 2002;46:111–153. PubMed

Wang Z., Wu M. Phylogenomic reconstruction indicates mitochondrial ancestor was an energy parasite. PLoS ONE. 2014;9:e110685. doi: 10.1371/journal.pone.0110685. PubMed DOI PMC

Larkum A.W.D., Lockhart P.J., Howe C.J. Shopping for plastid. Trends Plant. Sci. 2007;12:189–195. doi: 10.1016/j.tplants.2007.03.011. PubMed DOI

Sagan L. On the origin of mitosing cells. J. Theor. Biol. 1967;14:225–274. doi: 10.1016/0022-5193(67)90079-3. PubMed DOI

Goksøyr J. Evolution of eukaryotic cells. Nature. 1967;214:1161. doi: 10.1038/2141161a0. PubMed DOI

Margulis L. Symbiosis in evolution. Sci. Am. 1971;225:48–57. doi: 10.1038/scientificamerican0871-48. PubMed DOI

Lane N. Serial endosymbiosis or singular event at the origin of eucaryotes? J. Theor. Biol. 2017;434:58–67. doi: 10.1016/j.jtbi.2017.04.031. PubMed DOI

Kelly D.P. Autotrophy: Concepts of lithotrophic bacteria and their organic metabolism. Annu. Rev. Microbiol. 1971;25:177–210. doi: 10.1146/annurev.mi.25.100171.001141. PubMed DOI

Bodył A. Did some red alga-derived plastids evolved via kleptoplastidy? A hypothesis. Biol. Rev. 2018;93:201–222. doi: 10.1111/brv.12340. PubMed DOI

Logacheva M.D., Schelkunov M.I., Shtratnikova V.Y., Matveeva M.V., Penin A.A. Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives. Sci. Rep. 2016;6:30042. doi: 10.1038/srep30042. PubMed DOI PMC

Lavrov D.V., Pett W. Animal Mitochondrial DNA as We Do Not Know It: Mt-Genome Organization and Evolution in Nonbilaterian Lineages. Genom. Biol. Evol. 2016;8:2896–2913. doi: 10.1093/gbe/evw195. PubMed DOI PMC

Sobotka R., Esson H.J., Koník P., Trsková E., Moravcová L., Horák A., Dufková P., Oborník M. Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans. Sci. Rep. 2017;7:13214. doi: 10.1038/s41598-017-13575-x. PubMed DOI PMC

Nonoyama T., Kazamia E., Nawaly H., Gao X., Tsuji Y., Matsuda Y., Bowler C., Tanaka T.G., Dorrell R. Metabolic Innovations Underpinning the Origin and Diversification of the Diatom hloroplast. Biomolecules. 2019;9:322. doi: 10.3390/biom9080322. PubMed DOI PMC

Füssy Z., Faitová T., Oborník M. Subcellular Compartments Interplay for Carbon and Nitrogen Allocation in Chromera velia and Vitrella brassicaformis. Genom. Biol. Evol. 2019;11:1765–1779. doi: 10.1093/gbe/evz123. PubMed DOI PMC

Gray M.W., Lukeš J., Archibald J.M., Keeling P.J., Doolittle W.F. Irremediable complexity? Science. 2000;330:920–921. doi: 10.1126/science.1198594. PubMed DOI

Cavalier-Smith T., Lee J.J. Protozoa as Hosts for Endosymbioses and the Conversion of Symbionts into Organelles. J. Protozool. 1985;32:376–379. doi: 10.1111/j.1550-7408.1985.tb04031.x. DOI

Keeling P.J., Archibald J.M. Organelle Evolution: What’s in a Name? Curr. Biol. 2008;18:R345–R347. doi: 10.1016/j.cub.2008.02.065. PubMed DOI

Reyes-Prieto M., Latorre A., Moya A. Scanty microbes, the ‘symbionelle’ concept. Environ. Microbiol. 2014;16:335–338. doi: 10.1111/1462-2920.12220. PubMed DOI

van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A., Tiricz H., et al. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science. 2010;327:1122–1126. doi: 10.1126/science.1184057. PubMed DOI

Nowack E.C.M. Paulinella chromatophora – rethinking the transition from endosymbiont to organelle. Acta Soc. Bot. Pol. 2014;83:387–397. doi: 10.5586/asbp.2014.049. DOI

Husník F., Tashyreva D., Boscaro V., George E.E., Lukeš J., Keeling P.J. Bacterial and archaeal symbiosis with prostists. Curr. Biol. 2021;31:R1–R16. doi: 10.1016/j.cub.2021.05.049. PubMed DOI

Thompson A.W., Foster R.A., Krupke A., Carter B.J., Musat N., Vaulot D., Kuypers M.M.M., Zehr J.P. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science. 2012;337:1546–1550. doi: 10.1126/science.1222700. PubMed DOI

Nakayama T., Kamikawa R., Tanifuji G., Kashiyama Y., Ohkouchi N., Archibald J.M., Inagaki Y. Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle. Proc. Natl. Acad. Sci. USA. 2014;111:11407–11412. doi: 10.1073/pnas.1405222111. PubMed DOI PMC

Nakabachi A., Ishida K., Hongoh Y., Ohkuma M., Miyagishima S.Y. Aphid gene of bacterial origin encodes a protein transported to an obligate endosymbiont. Curr. Biol. 2014;24:R640–R641. doi: 10.1016/j.cub.2014.06.038. PubMed DOI

Tomas R.N., Cox E.R. Observations on symbiosis of Peridinium Balticum and its intracellular alga.1. Ultrastructure. J. Phycol. 1973;9:304–323.

Jeffrey S.W., Vesk M. Further evidence for a membrane bound endosymbiont within the dinoflagellate Peridinium foliaceum. J. Phycol. 1976;12:450–455.

Imanian B., Pombert J.-F., Dorrell R.G., Burki F., Keeling P.J. Tertiary Endosymbiosis in Two Dinotoms Has Generated Little Change in the Mitochondrial Genomes of Their Dinoflagellate Hosts and Diatom Endosymbionts. PLoS ONE. 2012;7:e43763. doi: 10.1371/journal.pone.0043763. PubMed DOI PMC

Complex Endosymbioses I: From Primary to Complex Plastids, Serial Endosymbiotic Events