Abstract
The evolution of eukaryotic photosynthesis marked a major transition for life on Earth, profoundly impacting the atmosphere of the Earth and evolutionary trajectory of an array of life forms. There are about ten lineages of photosynthetic eukaryotes, including Chloroplastida, Rhodophyta, and Cryptophyta. Mechanistically, eukaryotic photosynthesis arose via a symbiotic merger between a host eukaryote and either a cyanobacterial or eukaryotic photosymbiont. There are, however, many aspects of this major evolutionary transition that remain unsettled. The field, so far, has been dominated by proposals formulated following the principle of parsimony, such as the Archaeplastida hypothesis, in which a taxonomic lineage is often conceptually recognized as an individual cell (or a distinct entity). Such an assumption could lead to confusion or unrealistic interpretation of discordant genomic and phenotypic data. Here, we propose that the free-living ancestors to the plastids may have originated from a diversified lineage of cyanobacteria that were prone to symbioses, akin to some modern-day algae such as the Symbiodiniaceae dinoflagellates and Chlorella-related algae that associate with a number of unrelated host eukaryotes. This scenario, which assumes the plurality of ancestral form, better explains relatively minor but important differences that are observed in the genomes of modern-day eukaryotic algal species. Such a non-typological (or population-aware) way of thinking seems to better-model empirical data, such as discordant phylogenies between plastid and host eukaryote genes.
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Notes
- 1.
There are more recently identified cases of cyanobacterial integration into the eukaryotic cells, such as in the case of photosynthetic Paulinella species (Lhee et al. 2019) and rhopalodiacean diatoms (Nakayama and Inagaki 2017). It is, however, debated as to whether they should be called plastids (Keeling and Archibald 2008).
References
Adl SM, Bass D, Lane CE et al (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119
Bachmann A, Beard VL, McCarty PL (1985) Performance characteristics of the anaerobic baffled reactor. Water Res 19:99–106
Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977
Boulotte NM, Dalton SJ, Carroll AG et al (2016) Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J 10:2693–2701
Burki F, Kaplan M, Tikhonenkov DV et al (2016) Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc R Soc B Biol Sci 283:20152802
Cavalier-Smith T (1982) The origins of plastids. Biol J Linn Soc 17:289–306
Cenci U, Sibbald SJ, Curtis BA et al (2018) Nuclear genome sequence of the plastid-lacking cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids. BMC Biol 16:137
Delwiche CF, Palmer JD (1996) Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol 13:873–882
Desnitskiy A (2017) A symbiosis of amphibian embryos and larvae with unicellular green algae. Russ J Herpetol 24:223–227
Dumas E, Feurtey A, Rodríguez de la Vega RC et al (2020) Independent domestication events in the blue-cheese fungus Penicillium roqueforti. Mol Ecol (Early View online)
Gawryluk RMR, Tikhonenkov DV, Hehenberger E et al (2019) Non-photosynthetic predators are sister to red algae. Nature 572:240–243
Gomaa F, Kosakyan A, Heger TJ et al (2014) One alga to rule them all: unrelated mixotrophic testate amoebae (Amoebozoa, Rhizaria and Stramenopiles) share the same symbiont (Trebouxiophyceae). Protist 165:161–176
Hamada M, Schröder K, Bathia J et al (2018) Metabolic co-dependence drives the evolutionarily ancient Hydra–Chlorella symbiosis. elife 7:e35122
Hoshina R, Iwataki M, Imamura N (2010) Chlorella variabilis and Micractinium reisseri sp. nov. (Chlorellaceae, Trebouxiophyceae): redescription of the endosymbiotic green algae of Paramecium bursaria (Peniculia, Oligohymenophorea) in the 120th year. Phycol Res 58:188–201
Jassey VEJ, Signarbieux C, Hättenschwiler S et al (2015) An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Sci Rep 5:1–10
Kawaida H, Ohba K, Koutake Y et al (2013) Symbiosis between hydra and chlorella: molecular phylogenetic analysis and experimental study provide insight into its origin and evolution. Mol Phylogenet Evol 66:906–914
Keeling PJ, Archibald JM (2008) Organelle evolution: What’s in a name? Curr Biol 18:R345–R347
Kerney R, Kim E, Hangarter RP et al (2011) Intracellular invasion of green algae in a salamander host. Proc Natl Acad Sci 108:6497–6502
Kerney R, Leavitt J, Hill E et al (2019) Co-cultures of Oophila amblystomatis between Ambystoma maculatum and Ambystoma gracile hosts show host-symbiont fidelity. Symbiosis 78:73–85
Kessler E, Huss VAR, Rahat M (1988) Species-specific ability of Chlorella strains (Chlorophyceae) to form stable symbioses with Hydra viridis. Plant Syst Evol 160:241–246
Kim E, Lin Y, Kerney R et al (2014) Phylogenetic analysis of algal symbionts associated with four North American amphibian egg masses. PLoS One 9:e108915
Kobayakawa Y (2017) Symbiosis between green algae and hydra. In: Grube M, Muggia L, Seckenbach J (eds) Algal and cyanobacteria symbioses. World Scientific, London, pp 347–369
LaJeunesse TC, Parkinson JE, Gabrielson PW et al (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580
Lara E, Gomaa F (2017) Symbiosis between testate amoebae and photosynthetic organisms. In: Grube M, Muggia L, Seckenbach J (eds) Algal and cyanobacteria symbioses. World Scientific, London, pp 399–419
Lhee D, Ha J-S, Kim S et al (2019) Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species. Sci Rep 9:1–11
Lin Y, Bishop CD (2015) Identification of free-living Oophila amblystomatis (Chlorophyceae) from yellow spotted salamander and wood frog breeding habitat. Phycologia 54:183–191
Martin G, Joseph S, Lucia M (2016) Algal and cyanobacteria symbioses. World Scientific, London
Maruyama S, Kim E (2013) A modern descendant of early green algal phagotrophs. Curr Biol 23:1081–1084
Matthews JL, Crowder CM, Oakley CA et al (2017) Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proc Natl Acad Sci 114:13194–13199
Matthews JL, Oakley CA, Lutz A et al (2018) Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis. Proc R Soc B Biol Sci 285:20182336
McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959
Mies M, Sumida PYG, Rädecker N, Voolstra CR (2017) Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start? Front Ecol Evol 5:56
Moreira D, Le Guyader H, Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405:69–72
Muto K, Nishikawa K, Kamikawa R, Miyashita H (2017) Symbiotic green algae in eggs of Hynobius nigrescens, an amphibian endemic to Japan. Phycol Res 65:171–174
Nakayama T, Inagaki Y (2017) Genomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms. Sci Rep 7:1–8
Nema M, Hanson ML, Müller KM (2019) Phylogeny of the egg-loving green alga Oophila amblystomatis (Chlamydomonadales) and its response to the herbicides atrazine and 2,4-D. Symbiosis 77:23–39
Okamoto N, Inouye I (2005) A secondary symbiosis in progress? Science 310:287–287
Okamoto N, Inouye I (2006) Hatena arenicola gen. et sp. nov., a katablepharid undergoing probable plastid acquisition. Protist 157:401–419
Orr H (1888) Note on the development of amphibians, chiefly concerning the central nervous system; with additional observations on the hypophysis, mouth, and the appendages and skeleton of the head. Q J Microsc Sci New Ser 29:295–324
Pitsch G, Adamec L, Dirren S et al (2017) The green Tetrahymena utriculariae n. sp. (Ciliophora, Oligohymenophorea) with its endosymbiotic algae (Micractinium sp.), living in traps of a carnivorous aquatic plant. J Eukaryot Microbiol 64:322–335
Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2:e394
Pröschold T, Darienko T, Silva PC et al (2011) The systematics of Zoochlorella revisited employing an integrative approach. Environ Microbiol 13:350–364
Rodríguez-Ezpeleta N, Brinkmann H, Burey SC et al (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15:1325–1330
Rueckert S, Betts EL, Tsaousis AD (2019) The symbiotic spectrum: where do the gregarines fit? Trends Parasitol 35:687–694
Small DP, Bennett RS, Bishop CD (2014) The roles of oxygen and ammonia in the symbiotic relationship between the spotted salamander Ambystoma maculatum and the green alga Oophila amblystomatis during embryonic development. Symbiosis 64:1–10
Sproles AE, Oakley CA, Matthews JL et al (2019) Proteomics quantifies protein expression changes in a model cnidarian colonised by a thermally tolerant but suboptimal symbiont. ISME J 13:2334–2345
Strassert JFH, Jamy M, Mylnikov AP et al (2019) New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life. Mol Biol Evol 36:757–765
Stroud JT, Losos JB (2020) Bridging the process-pattern divide to understand the origins and early stages of adaptive radiation: a review of approaches with insights from studies of Anolis lizards. J Hered 111:33–42
Summerer M, Sonntag B, Sommaruga R (2007) An experimental test of the symbiosis specificity between the ciliate Paramecium bursaria and strains of the unicellular green alga Chlorella. Environ Microbiol 9:2117–2122
Tonooka Y, Watanabe T (2002) A natural strain of Paramecium bursaria lacking symbiotic algae. Eur J Protistol 38:55–58
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Maruyama, S., Kim, E. (2020). Evolution of Photosynthetic Eukaryotes; Current Opinion, Perplexity, and a New Perspective. In: Kloc, M. (eds) Symbiosis: Cellular, Molecular, Medical and Evolutionary Aspects. Results and Problems in Cell Differentiation, vol 69. Springer, Cham. https://doi.org/10.1007/978-3-030-51849-3_12
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