Photosynthesis is a biochemical process essential for life, serving as the ultimate source of chemical energy for phototrophic and heterotrophic life forms. Since the machinery of the photosynthetic electron transport chain is quite complex and is unlikely to have evolved multiple independent times, it is believed that this machinery has been transferred to diverse eukaryotic organisms by endosymbiotic events involving a eukaryotic host and a phototrophic endosymbiont. Thus, photoautotrophy, as a benefit, is transmitted through the evolution of plastids. However, many eukaryotes became secondarily heterotrophic, reverting to hetero-osmotrophy, phagotrophy, or parasitism. Here, I briefly review the constructive evolution of plastid endosymbioses and the consequential switch to reductive evolution involving losses of photosynthesis and plastids and the evolution of parasitism from a photosynthetic ancestor.

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

Institute of Parasitology Biology Centre CAS 37005 České Budějovice Czech Republic

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Shih P.M. Cyanobacterial evolution: Fresh insight into ancient questions. Curr. Biol. 2015;25:R193. doi: 10.1016/j.cub.2014.12.046. PubMed DOI

Shih P.M., Matzke J. Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl. Acad. Sci USA. 2013;110:12355–12360. doi: 10.1073/pnas.1305813110. PubMed DOI PMC

Mereschkowksy C. Ober Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Zentralbl. 1905;25:593–604.

Martin W., Kowallik K.V. Annotated English translation of of Mereschkowsky’s 1905 paper “Über natur und Ursprung der Chromatophoren im Pflanzenreiche”. Eur. J. Phycol. 1999;34:287–295. doi: 10.1017/S0967026299002231. DOI

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. Microbial Cell. 2019;6:134–141. doi: 10.15698/mic2019.02.669. PubMed DOI PMC

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

Gould S.B., Waller R.F., McFadden G.I. Plastid evolution. Ann. 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. Microbial Cell. 2019;6:123–133. doi: 10.15698/mic2019.02.668. PubMed DOI PMC

Keeling P.J. Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 2004;91:1481–1493. doi: 10.3732/ajb.91.10.1481. PubMed DOI

Jackson C., Clayden S., Reyes-Prieto A. The Glaucophyta: The blue-green plants in a nutshell. Acta Soc. Bot. Pol. 2015;84:149–165. doi: 10.5586/asbp.2015.020. DOI

Maréchal E., editor. Primary Endosymbiosis: Emergence of Primary Chloroplasts and Chromatophore Two Independent Events. Vol. 1829 Humana Press; New York, NY, USA: 2018. Plastids: Methods and protocols. Methods in molecular biology. PubMed

Larkum A.W.D., Kühl M. Chlorophyll d: The puzzle resolved. Trends Plant. Sci. 2005;10:P355–P357. doi: 10.1016/j.tplants.2005.06.005. PubMed DOI

Martin W., Herrmann R.G. Gene transfer from organelles to the nucleus: How much, what happens, and why? Plant. Phys. 1998;118:9–17. doi: 10.1104/pp.118.1.9. PubMed DOI PMC

Oborník M., Green B. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol. Biol. Evol. 2005;22:2343–2353. doi: 10.1093/molbev/msi230. PubMed DOI

Cihlář J., Füssy Z., Oborník M. Evolution of tetrapyrrole pathway in eukaryotic phototrophs. Adv. Bot. Res. 2019;90:273–309.

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

Stiller J.W., Reel D.C., Johnson J.C. A single origin of plastids revisited: Convergent evolution in organellar genome content. J. Phycol. 2003;39:95–105. doi: 10.1046/j.1529-8817.2003.02070.x. 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. Eukaryot. Microbiol. 1999;46:347–366. doi: 10.1111/j.1550-7408.1999.tb04614.x. PubMed DOI

Marin B., Nowack E.C.M., 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

Yoon H.S., Reyes-Prieto A., Melkonian M., Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont. Curr. Biol. 2006;16:R670–R672. doi: 10.1016/j.cub.2006.08.018. PubMed DOI

Delaye L., Valadez-Cano C., Pérez-Zamorano B. How really ancient is Paulinella chromatophora? PLoS Curr. Tree of Life. 2016:1. doi: 10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b. PubMed DOI PMC

Delwiche C.F., Palmer J.D. The Origin Plastids and Their Spread via Secondary Symbiosis Plant Systematics and Evolution. Suppl. 11 Springer; Berlin, Germany: 1997. pp. 53–86.

Delwiche C.F. Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 1999;154:S164–S177. doi: 10.1086/303291. PubMed DOI

Falkowski P.G., Katz M.E., Knoll A.H., Quigg A., Raven J.A., Schofield O., Taylor F.J. The evolution of modern phytoplankton. Science. 2004;305:354–360. doi: 10.1126/science.1095964. PubMed DOI

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

Curtis B., Tanifuji G., Burki F., Gruber A., Irimia M., Maruyama S., Arias M., Ball S., Gile G., Hirakawa Y., et al. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature. 2012;492:59–65. doi: 10.1038/nature11681. PubMed DOI

Vanclová A.M.G., Hadariová L., Hrdá Š., Hampl V. Secondary plastids of euglenophytes. Adv. Bot. Res. 2017;84:321–358.

Matsumoto T., Shinozaki F., Chikuni T., Yabuki A., Takishita K., Kawachi M., Nakayama T., Inouye I., Hashimoto T., Inagaki Y. Green-colored plastids in the dinoflagellate genus Lepidodinium are of core chlorophyte origin. Protist. 2011;162:268–276. doi: 10.1016/j.protis.2010.07.001. PubMed DOI

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

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

Cavalier-Smith T. Kingdom Chromista and its eight phyla: A new synthesis emphasising periplastid protein targeting, cyto-skeletal and periplastid evolution, and ancient divergences. Protoplasma. 2018;255:297–357. doi: 10.1007/s00709-017-1147-3. PubMed DOI PMC

Bodył A., Stiller J.W., Mackiewicz P. Chromalveolate plastids: Direct descents or multiple endosymbioses? Trends 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. Com. 2014;5:5764. doi: 10.1038/ncomms6764. PubMed DOI PMC

Petersen J., Ludewig A.K., Michael V., Bunk B., Jarek M., Baurain D., Brinkmann 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 D.R., Bowler C. Secondary plastids of stramenopiles. Adv. Bot. Res. 2017;84:57–103.

Moore C.E., Archibald J.M. Nucleomorph genomes. Ann. Rev. Genet. 2009;43:251–264. doi: 10.1146/annurev-genet-102108-134809. PubMed DOI

Oborník M., Modrý D., Lukeš M., Černotíková-Stříbrná E., Cihlář J., Tesařová M., Kotabová E., Vancová E., Prášil O., Lukeš J. Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist. 2012;163:306–323. doi: 10.1016/j.protis.2011.09.001. PubMed DOI

Ševčíková T., Horák A., Klimeš V., Zbránková V., Demir-Hilton E., Sudek S., Jenkins J., Schmutz J., Přibyl P., Fousek J., et al. Updating algal evolutionary relationships through plastid genome sequencing: Did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci. Rep. 2015;5:10134. doi: 10.1038/srep10134. 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

Oborník M., Janouškovec J., Chrudimský T., Lukeš J. Evolution of the apicoplast and its host: From heterotrophy to autotrophy and back again. Int. J. Parasitol. 2009;39:1–12. doi: 10.1016/j.ijpara.2008.07.010. PubMed DOI

Pospíšil P. Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim. Biophys. Acta. 2012;1817:218–231. doi: 10.1016/j.bbabio.2011.05.017. PubMed DOI

Koblížek M., Zeng Y., Horák A., Oborník M. Regressive evolution of photosynthesis in the Roseobacter clade. Adv. Bot. Res. 2013;66:385–405.

Hadariová L., Vesteg M., Hampl V., Krajčovič 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

Votýpka J., Nodrý D., Oborník M., Šlapeta J., Lukeš J. Apicomplexa. In: Archibald J.M., Simpson G.B., Slamovits C.H., editors. Handbook of the Protists. Springer; Berlin, Germany: 2017. pp. 567–624.

Těšitel J. Functional biology of parasitic plants: A review. Plant. Ecol. Evol. 2017;149:5–20. doi: 10.5091/plecevo.2016.1097. DOI

De la Cruz V.F., Gittleson S.M. The genus Polytomella: A review of classification, morphology, life cycle, metabolism, and motility. Arch. Protistenkunde. 1981;124:1–28. doi: 10.1016/S0003-9365(81)80001-2. DOI

Boucias D.G., Becnel J.J., White S.E., Bott M. In vivo and in vitro development of the protist Helicosporidium sp. J. Eukaryot. Microbiol. 2001;48:460–470. doi: 10.1111/j.1550-7408.2001.tb00180.x. 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

Blouin N.A., Lane C.E. Red algae provide fertile ground for exploring parasite evolution. Persp. Phycol. 2016;2016. 3:11–19. doi: 10.1127/pip/2015/0027. DOI

Marin B., Palm A., Klingberg M., Melkonian M. Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorhic signatures in the SSU rRNA secondary structure. Protist. 2003;154:99–145. doi: 10.1078/143446103764928521. PubMed DOI

Lowe C.D., Keeling P.J., Martin L.E., Slamovits C.H., Watts P.C., Montagnes D.J.S. Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. J. Plankton Res. 2011;33:555–567. doi: 10.1093/plankt/fbq110. DOI

Füssy Z., Oborník M. Chromerids and their plastids. Adv. Bot. Res. 2017;84:187–218.

Füssy Z., Oborník M. Plastids: Methods and protocols methods in molecular biology. In: Maréchal E., editor. Complex Endosymbioses I: From Primary to Complex Plastids, Multiple Independent Events. Vol. 1829. Humana Press; New York, NY, USA: 2018. pp. 17–35. PubMed

Sato S. The apicomplexan plastid and its evolution. Cell. Mol. Life Sci. 2011;68:1285–1296. doi: 10.1007/s00018-011-0646-1. PubMed DOI PMC

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

Gornik S.G., Febrimarsa A.M.C., 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

Burki F. The convoluted evolution of eukaryotes with complex plastids. Adv. Bot. Res. 2017;84:1–30.

Stoecker D.K., Hansen P.J., Caron D.A., Mitra A. Mixotrophy in the marine plankton. Ann. Rev. Mar. Sci. 2016;9:311–335. doi: 10.1146/annurev-marine-010816-060617. PubMed DOI

Rezic T., Filipović J., Santec B. Photo-mixotrophic cultivation of algae Euglena gracilis for lipid production. Agr. Consp. Sci. 2013;2013 78:65–69.

Heredia-Arroyo T., Wei W., Hu B. Mixotrophic cultivation of Chlorella vulgaris and its potential application for the oil accumulation from non-sugar materials. Biomass Bioenerg. 2011;35:2245–2253. doi: 10.1016/j.biombioe.2011.02.036. DOI

Villanova V., Fortunato A.E., Singh D., Bo D.D., Conte M., Obata T., Jouhet J., Fernie A.R., Maréchal E., Falciatore A., et al. Investigating mixotrophic metabolism in the model diatom Phaeodactylum tricornutum. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017;372:20160404. doi: 10.1098/rstb.2016.0404. PubMed DOI PMC

Jeong J.H., Yoo Y.D., Kim J.S., Seong K.A., Kang N.S., Kim T.H. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 2010;45:65–91. doi: 10.1007/s12601-010-0007-2. DOI

McFadden G.I., Reith M.E., Munholland J., Lang-Unnasch N. Plastid in human parasites. Nature. 1996;381:482. doi: 10.1038/381482a0. PubMed DOI

McFadden G.I., Waller R.F. Plastids in parasites of humans. Bioessays. 1997;19:1033–1040. doi: 10.1002/bies.950191114. PubMed DOI

Moore R.B., Oborník M., Janouškovec J., Chrudimský T., Vancová M., Green D., Wright S., Davies N., Bolch C., Heimann K., et al. A photosynthetic alveolate closely related to apicomplexan parasites. Nature. 2008;451:959–963. doi: 10.1038/nature06635. PubMed DOI

Woo Y., Ansari H., Otto T.D., Klinger C., Kolísko M., Saxena A., Shanmugam D., Tayyrov A., Veluchamy A., Ali S., et al. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. elife. 2015;4:e06974. doi: 10.7554/eLife.06974. PubMed DOI PMC

Janouškovec J., Tikhonenkov D.V., Burki F., Howe A.T., Kolísko M., Mylnikov A.P., Keeling P.J. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc. Natl. Acad. Sci. USA. 2015;112:10200–10207. doi: 10.1073/pnas.1423790112. PubMed DOI PMC

Kořený L., Sobotka R., Janouškovec J., Keeling P.J., Oborník M. Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant. Cell. 2011;23:3454–3462. doi: 10.1105/tpc.111.089102. PubMed DOI PMC

Okamoto N., McFadden G.I. The mother of all parasites. Futur. Microbiol. 2008;3:391–395. doi: 10.2217/17460913.3.4.391. DOI

Janouškovec J., Horák A., Barott K.L., Rohwer F.L., Keeling P.J. Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr. Biol. 2012;22:R518–R519. doi: 10.1016/j.cub.2012.04.047. PubMed DOI

Janouškovec J., Horák A., Barott K.L., Rohwer F.L., Keeling P.J. Environmental distribution of coral-associated relatives of apicomplexan parasites. ISME J. 2013;7:444–447. doi: 10.1038/ismej.2012.129. PubMed DOI PMC

Cumbo V.R., Baird A.H., Moore R.B., Negri A.P., Neilan B.A., Salih A., van Oppen M.J., Marquis C.P. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. Protist. 2013;164:237–244. doi: 10.1016/j.protis.2012.08.003. PubMed DOI

Mohamed A.R., Cumbo V.R., Harii A., Shizato C., Chan C.X., Ragan M.A., Satoh N., Ball E.E., Miller D.J. Deciphering the nature of the coral-Chromera association. ISME J. 2018;12:776–790. doi: 10.1038/s41396-017-0005-9. PubMed DOI PMC

Skovgaard A., Karpov S.A., Guillou L. The parasitic dinoflagellates Blastodinium spp. Inhabiting the gut of marine, plaktonic copepods: Morphology, ecology, and unrecognized species diversity. Front. Microbiol. 2012;3:305. doi: 10.3389/fmicb.2012.00305. PubMed DOI PMC

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

Kwong W.K., Del Campo J., Mathur V., Vermeij M.J.A., Keeling P.J. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature. 2019;568:103–107. doi: 10.1038/s41586-019-1072-z. PubMed DOI

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