Photosymbiosis

Lichens represent an association between one or more fungal mycobionts and one or more photosynthetic algal or cyanobacterial photobionts. The mycobiont provides protection from predation and desiccation, while the photobiont provides energy in the form of fixed carbon. Cyanobacterial partners are also capable of fixing nitrogen for the fungal partner.{{Cite journal |last1=Spribille |first1=Toby |last2=Resl |first2=Philipp |last3=Stanton |first3=Daniel E. |last4=Tagirdzhanova |first4=Gulnara |date=June 2022 |title=Evolutionary biology of lichen symbioses |journal=New Phytologist |language=en |volume=234 |issue=5 |pages=1566–1582 |doi=10.1111/nph.18048 |pmid=35302240 |issn=0028-646X|doi-access=free |bibcode=2022NewPh.234.1566S }} Recent work suggests that non-photosynthetic bacterial microbiomes associated with lichens may also have functional significance to lichens.{{Cite journal |last1=Grube |first1=Martin |last2=Cernava |first2=Tomislav |last3=Soh |first3=Jung |last4=Fuchs |first4=Stephan |last5=Aschenbrenner |first5=Ines |last6=Lassek |first6=Christian |last7=Wegner |first7=Uwe |last8=Becher |first8=Dörte |last9=Riedel |first9=Katharina |last10=Sensen |first10=Christoph W |last11=Berg |first11=Gabriele |date=2015-02-01 |title=Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics |journal=The ISME Journal |language=en |volume=9 |issue=2 |pages=412–424 |doi=10.1038/ismej.2014.138 |issn=1751-7362 |pmc=4303634 |pmid=25072413|bibcode=2015ISMEJ...9..412G }}

Most mycobiont partners derive from the ascomycetes, and the largest class of lichenized fungi is Lecanoromycetes.{{Cite journal |last1=Miadlikowska |first1=Jolanta |last2=Kauff |first2=Frank |last3=Högnabba |first3=Filip |last4=Oliver |first4=Jeffrey C. |last5=Molnár |first5=Katalin |last6=Fraker |first6=Emily |last7=Gaya |first7=Ester |last8=Hafellner |first8=Josef |last9=Hofstetter |first9=Valérie |last10=Gueidan |first10=Cécile |last11=Otálora |first11=Mónica A.G. |last12=Hodkinson |first12=Brendan |last13=Kukwa |first13=Martin |last14=Lücking |first14=Robert |last15=Björk |first15=Curtis |date=October 2014 |title=A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families |journal=Molecular Phylogenetics and Evolution |language=en |volume=79 |pages=132–168 |doi=10.1016/j.ympev.2014.04.003 |pmc=4185256 |pmid=24747130|bibcode=2014MolPE..79..132M |hdl=11336/11976 }} The vast majority of lichens derive photobionts from Chlorophyta (green algae). The co-evolutionary dynamics between mycobionts and photobionts are still unclear, as many photobionts are capable of free-living, and many lichenized fungi display traits adaptive to lichenization such as the capacity to withstand higher levels of reactive oxygen species (ROS), the conversion of sugars to polypols that help withstand dedication, and the downregulation of fungal virulence. However, it is still unclear whether these are derived or ancestral traits.

Currently described photobiont species number about 100, far less than the 19,000 described species of fungal mycobionts, and factors such as geography can predominate over mycobiont preference.{{Cite journal |last1=Yahr |first1=Rebecca |last2=Vilgalys |first2=Rytas |last3=DePriest |first3=Paula T. |date=September 2006 |title=Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis |url=https://nph.onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2006.01792.x |journal=New Phytologist |language=en |volume=171 |issue=4 |pages=847–860 |doi=10.1111/j.1469-8137.2006.01792.x |pmid=16918555 |bibcode=2006NewPh.171..847Y |issn=0028-646X}}{{Cite journal |last1=Sanders |first1=William B. |last2=Masumoto |first2=Hiroshi |date=September 2021 |title=Lichen algae: the photosynthetic partners in lichen symbioses |journal=The Lichenologist |language=en |volume=53 |issue=5 |pages=347–393 |doi=10.1017/S0024282921000335 |issn=0024-2829|doi-access=free |bibcode=2021ThLic..53..347S }} Phylogenetic analyses in lichenized fungi have suggested that, throughout evolutionary history, there has been repeated loss of photosymbionts, switching of photosymbionts, and independent lichenization events in previously unrelated fungal taxa.{{Cite journal |last1=Nelsen |first1=Matthew P. |last2=Lücking |first2=Robert |last3=Boyce |first3=C. Kevin |last4=Lumbsch |first4=H. Thorsten |last5=Ree |first5=Richard H. |date=September 2020 |title=The macroevolutionary dynamics of symbiotic and phenotypic diversification in lichens |journal=Proceedings of the National Academy of Sciences |language=en |volume=117 |issue=35 |pages=21495–21503 |doi=10.1073/pnas.2001913117 |doi-access=free |issn=0027-8424 |pmc=7474681 |pmid=32796103|bibcode=2020PNAS..11721495N }} Loss of lichenization has likely led to the coexistence of non-lichenized fungi and lichenized fungi in lichens.

Sponges (phylum Porifera) have a large diversity of photosymbiote associations. Photosymbiosis is found in four classes of Porifera (Demospongiae, Hexactinellida, Homoscleromorpha, and Calcarea), and known photosynthetic partners are cyanobacteria, chloroflexi, dinoflagellates, and red (Rhodophyta) and green (Chlorophyta) algae. Relatively little is known about the evolutionary history of sponge photosymbiois due to a lack of genomic data.{{Cite journal |last1=Melo Clavijo |first1=Jenny |last2=Donath |first2=Alexander |last3=Serôdio |first3=João |last4=Christa |first4=Gregor |date=November 2018 |title=Polymorphic adaptations in metazoans to establish and maintain photosymbioses |journal=Biological Reviews |language=en |volume=93 |issue=4 |pages=2006–2020 |doi=10.1111/brv.12430 |pmid=29808579 |issn=1464-7931|doi-access=free }} However, it has been shown that photosymbiotes are acquired vertically (transmission from parent to offspring) and/or horizontally (acquired from the environment).{{Cite journal |last1=de Oliveira |first1=Bruno Francesco Rodrigues |last2=Freitas-Silva |first2=Jéssyca |last3=Sánchez-Robinet |first3=Claudia |last4=Laport |first4=Marinella Silva |date=December 2020 |title=Transmission of the sponge microbiome: moving towards a unified model |url=https://sfamjournals.onlinelibrary.wiley.com/doi/10.1111/1758-2229.12896 |journal=Environmental Microbiology Reports |language=en |volume=12 |issue=6 |pages=619–638 |doi=10.1111/1758-2229.12896 |pmid=33048474 |bibcode=2020EnvMR..12..619D |issn=1758-2229|url-access=subscription }} Photosymbiotes can supply up to half of the host sponge's respiratory demands and can support sponges during times of nutrient stress.{{Cite journal |last1=Hudspith |first1=Meggie |last2=de Goeij |first2=Jasper M |last3=Streekstra |first3=Mischa |last4=Kornder |first4=Niklas A |last5=Bougoure |first5=Jeremy |last6=Guagliardo |first6=Paul |last7=Campana |first7=Sara |last8=van der Wel |first8=Nicole N |last9=Muyzer |first9=Gerard |last10=Rix |first10=Laura |date=2022-06-02 |title=Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge |url=https://doi.org/10.1038/s41396-022-01254-3 |journal=The ISME Journal |volume=16 |issue=9 |pages=2076–2086 |doi=10.1038/s41396-022-01254-3 |issn=1751-7362 |pmc=9381825 |pmid=35654830|bibcode=2022ISMEJ..16.2076H }}

Members of certain classes in phylum Cnidaria are known for photosymbiotic partnerships. Members of corals (Class Anthozoa) in the orders Hexacorallia and Octocorallia form well-characterized partnerships with the dinoflagellate genus Symbiodinium. Some jellyfish (class Scyphozoa) in the genus Cassiopea (upside-down jellyfish) also possess Symbiodinium. Certain species in the genus Hydra (class Hydrozoa) also harbor green algae and form a stable photosymbiosis.

The evolution of photosymbiosis in corals was likely critical for the global establishment of coral reefs.{{Cite journal |last1=Muscatine |first1=Leonard |last2=Goiran |first2=Claire |last3=Land |first3=Lynton |last4=Jaubert |first4=Jean |last5=Cuif |first5=Jean-Pierre |last6=Allemand |first6=Denis |date=February 2005 |title=Stable isotopes (δ 13 C and δ 15 N) of organic matrix from coral skeleton |journal=Proceedings of the National Academy of Sciences |language=en |volume=102 |issue=5 |pages=1525–1530 |doi=10.1073/pnas.0408921102 |doi-access=free |issn=0027-8424 |pmc=547863 |pmid=15671164}} Corals are likewise adapted to eject damaged photosymbionts that generate high levels of toxic reactive oxygen species, a process known as bleaching.{{Cite journal |last=Weis |first=Virginia M. |date=2008-10-01 |title=Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis |url=https://journals.biologists.com/jeb/article/211/19/3059/18247/Cellular-mechanisms-of-Cnidarian-bleaching-stress |journal=Journal of Experimental Biology |language=en |volume=211 |issue=19 |pages=3059–3066 |doi=10.1242/jeb.009597 |pmid=18805804 |bibcode=2008JExpB.211.3059W |issn=1477-9145}} The identity of the Symbiodinium photosymbiont can change in corals, although this depends largely on the mode of transmission: some species vertically transmit their algal partners through their eggs,{{Cite journal |last1=Padilla-Gamiño |first1=Jacqueline L. |last2=Pochon |first2=Xavier |last3=Bird |first3=Christopher |last4=Concepcion |first4=Gregory T. |last5=Gates |first5=Ruth D. |date=2012-06-06 |title=From Parent to Gamete: Vertical Transmission of Symbiodinium (Dinophyceae) ITS2 Sequence Assemblages in the Reef Building Coral Montipora capitata |journal=PLOS ONE |language=en |volume=7 |issue=6 |pages=e38440 |doi=10.1371/journal.pone.0038440 |doi-access=free |issn=1932-6203 |pmc=3368852 |pmid=22701642|bibcode=2012PLoSO...738440P }} while other species acquire environmental dinoflagellates as newly-released eggs.{{Cite journal |last1=van Oppen |first1=Madeleine J. H. |last2=Medina |first2=Mónica |date=2020-09-28 |title=Coral evolutionary responses to microbial symbioses |journal=Philosophical Transactions of the Royal Society B: Biological Sciences |language=en |volume=375 |issue=1808 |pages=20190591 |doi=10.1098/rstb.2019.0591 |issn=0962-8436 |pmc=7435167 |pmid=32772672}} Since algae are not preserved in the coral fossil record, understanding the evolutionary history of the symbiosis is difficult.{{Citation |last1=Stanley |first1=G. D. |title=The Evolution of the Coral–Algal Symbiosis |date=2009 |work=Coral Bleaching |volume=205 |pages=7–19 |editor-last=van Oppen |editor-first=Madeleine J. H. |url=http://link.springer.com/10.1007/978-3-540-69775-6_2 |access-date=2024-05-08 |place=Berlin, Heidelberg |publisher=Springer Berlin Heidelberg |language=en |doi=10.1007/978-3-540-69775-6_2 |isbn=978-3-540-69774-9 |last2=van de Schootbrugge |first2=B. |editor2-last=Lough |editor2-first=Janice M.|url-access=subscription }}  

In basal bilaterians, photosymbiosis in marine or brackish systems is present only in the family Convolutidae.{{Cite journal |last1=Paps |first1=J. |last2=Baguna |first2=J. |last3=Riutort |first3=M. |date=2009-07-14 |title=Bilaterian Phylogeny: A Broad Sampling of 13 Nuclear Genes Provides a New Lophotrochozoa Phylogeny and Supports a Paraphyletic Basal Acoelomorpha |url=http://dx.doi.org/10.1093/molbev/msp150 |journal=Molecular Biology and Evolution |volume=26 |issue=10 |pages=2397–2406 |doi=10.1093/molbev/msp150 |pmid=19602542 |issn=0737-4038}} In the group Acoela there is limited knowledge on the symbionts present, and they have been vaguely identified as zoochlorella or zooxanthella.{{Cite journal |last1=SHANNON |first1=THOMAS |last2=ACHATZ |first2=JOHANNES G. |date=2007-07-12 |title=Convolutriloba macropyga sp. nov., an uncommonly fecund acoel (Acoelomorpha) discovered in tropical aquaria |url=http://dx.doi.org/10.11646/zootaxa.1525.1.1 |journal=Zootaxa |volume=1525 |issue=1 |doi=10.11646/zootaxa.1525.1.1 |issn=1175-5334|url-access=subscription }}{{Cite journal |last=Ax |first=P. |date=April 1970 |title=Neue Pogaina-Arten (Turbellaria, Dalyellioda) mit Zooxanthellen aus dem Mesopsammal der Nordsee- und Mittelmeerküste |url=http://dx.doi.org/10.1007/bf00346899 |journal=Marine Biology |volume=5 |issue=4 |pages=337–340 |doi=10.1007/bf00346899 |bibcode=1970MarBi...5..337A |issn=0025-3162|url-access=subscription }} Some species have a symbiotic relationship with the chlorophyte Tetraselmis convolutae while others have a symbiotic relationship with the dinoflagellates Symbiodinium, Amphidinium klebsii, or diatoms in the genus Licomorpha.{{Cite journal |last1=Gschwentner |first1=Robert |last2=Mueller |first2=Johann |last3=Ladurner |first3=Peter |last4=Rieger |first4=Reinhard |last5=Tyler |first5=Seth |date=2003-02-12 |title=Unique patterns of longitudinal body-wall musculature in the Acoela (Plathelminthes): the ventral musculature of Convolutriloba longifissura |url=http://dx.doi.org/10.1007/s00435-003-0074-3 |journal=Zoomorphology |volume=122 |issue=2 |pages=87–94 |doi=10.1007/s00435-003-0074-3 |issn=0720-213X|url-access=subscription }}{{Cite journal |last1=Serôdio |first1=João |last2=Silva |first2=Raquel |last3=Ezequiel |first3=João |last4=Calado |first4=Ricardo |date=2010-07-14 |title=Photobiology of the symbiotic acoel flatwormSymsagittifera roscoffensis: algal symbiont photoacclimation and host photobehaviour |url=http://dx.doi.org/10.1017/s0025315410001001 |journal=Journal of the Marine Biological Association of the United Kingdom |volume=91 |issue=1 |pages=163–171 |doi=10.1017/s0025315410001001 |issn=0025-3154|url-access=subscription }}{{Cite journal |last=Taylor |first=D. L. |date=May 1971 |title=On the symbiosis betweenAmphidinium klebsii[Dinophyceae] andAmphiscolops langerhansi[Turbellaria: Acoela] |url=http://dx.doi.org/10.1017/s0025315400031799 |journal=Journal of the Marine Biological Association of the United Kingdom |volume=51 |issue=2 |pages=301–313 |doi=10.1017/s0025315400031799 |bibcode=1971JMBUK..51..301T |issn=0025-3154|url-access=subscription }}{{Cite journal |last1=Lopes |first1=Rubens Mendes |last2=Silveira |first2=Marina |date=July 1994 |title=Symbiosis between a pelagic flatworm and a dinoflagellate from a tropical area: structural observations |url=http://dx.doi.org/10.1007/bf00006376 |journal=Hydrobiologia |volume=287 |issue=3 |pages=277–284 |doi=10.1007/bf00006376 |bibcode=1994HyBio.287..277L |issn=0018-8158|url-access=subscription }}{{Cite journal |last1=Barneah |first1=Orit |last2=Brickner |first2=Itzchak |last3=Hooge |first3=Matthew |last4=Weis |first4=Virginia M. |last5=Benayahu |first5=Yehuda |date=2007-08-14 |title=First evidence of maternal transmission of algal endosymbionts at an oocyte stage in a triploblastic host, with observations on reproduction inWaminoa brickneri(Acoelomorpha) |url=http://dx.doi.org/10.1111/j.1744-7410.2007.00082.x |journal=Invertebrate Biology |volume=126 |issue=2 |pages=113–119 |doi=10.1111/j.1744-7410.2007.00082.x |bibcode=2007InvBi.126..113B |issn=1077-8306}}{{Cite journal |last1=Hikosaka-Katayama |first1=Tomoe |last2=Koike |first2=Kanae |last3=Yamashita |first3=Hiroshi |last4=Hikosaka |first4=Akira |last5=Koike |first5=Kazuhiko |date=September 2012 |title=Mechanisms of Maternal Inheritance of Dinoflagellate Symbionts in the Acoelomorph WormWaminoa litus |url=http://dx.doi.org/10.2108/zsj.29.559 |journal=Zoological Science |volume=29 |issue=9 |pages=559–567 |doi=10.2108/zsj.29.559 |pmid=22943779 |issn=0289-0003}}{{Cite journal |last=Apelt |first=G. |date=June 1969 |title=Die Symbiose zwischen dem acoelen Turbellar Convoluta convoluta und Diatomeen der Gattung Licmophora |url=http://dx.doi.org/10.1007/bf00353437 |journal=Marine Biology |volume=3 |issue=2 |pages=165–187 |doi=10.1007/bf00353437 |bibcode=1969MarBi...3..165A |issn=0025-3162|url-access=subscription }}{{Cite journal |last1=Ax |first1=Peter |last2=Apelt |first2=Gieselbert |date=1965 |title=Die ?Zooxanthellen? vonConvoluta convoluta (Turbellaria Acoela) entstehen aus Diatomeen |url=http://dx.doi.org/10.1007/bf00627043 |journal=Die Naturwissenschaften |volume=52 |issue=15 |pages=444–446 |doi=10.1007/bf00627043 |issn=0028-1042|url-access=subscription }}

In freshwater systems, photosymbiosis is present in platyhelminths belonging to the Rhabdocoela group.{{Cite journal |last1=Melo Clavijo |first1=Jenny |last2=Donath |first2=Alexander |last3=Serôdio |first3=João |last4=Christa |first4=Gregor |date=November 2018 |title=Polymorphic adaptations in metazoans to establish and maintain photosymbioses |journal=Biological Reviews |language=en |volume=93 |issue=4 |pages=2006–2020 |doi=10.1111/brv.12430 |pmid=29808579 |issn=1464-7931|doi-access=free }} In this group, members of the Provorticidae, Dalyeliidae, and Typhloplanidae families are symbiotic.{{Cite journal |last=Ax |first=P. |date=April 1970 |title=Neue Pogaina-Arten (Turbellaria, Dalyellioda) mit Zooxanthellen aus dem Mesopsammal der Nordsee- und Mittelmeerküste |url=http://dx.doi.org/10.1007/bf00346899 |journal=Marine Biology |volume=5 |issue=4 |pages=337–340 |doi=10.1007/bf00346899 |bibcode=1970MarBi...5..337A |issn=0025-3162|url-access=subscription }} Members of Provorticidae likely feed on diatoms and retain their symbionts.{{Cite journal |last=Ax |first=P. |date=April 1970 |title=Neue Pogaina-Arten (Turbellaria, Dalyellioda) mit Zooxanthellen aus dem Mesopsammal der Nordsee- und Mittelmeerküste |url=http://dx.doi.org/10.1007/bf00346899 |journal=Marine Biology |volume=5 |issue=4 |pages=337–340 |doi=10.1007/bf00346899 |bibcode=1970MarBi...5..337A |issn=0025-3162|url-access=subscription }} Typhloplanidae have symbiotic relationships with the chlorophytes in the genus Chlorella.{{Cite journal |last=Douglas |first=Angela E. |date=June 1987 |title=Experimental studies on symbioticChlorellain the Neorhabdocoel TurbellariaDalyellia viridisandTyphloplana viridata |url=http://dx.doi.org/10.1080/00071618700650181 |journal=British Phycological Journal |volume=22 |issue=2 |pages=157–161 |doi=10.1080/00071618700650181 |issn=0007-1617|url-access=subscription }}

Photosymbiosis is taxonomically restricted in Mollusca.{{Cite journal |last1=Melo Clavijo |first1=Jenny |last2=Donath |first2=Alexander |last3=Serôdio |first3=João |last4=Christa |first4=Gregor |date=November 2018 |title=Polymorphic adaptations in metazoans to establish and maintain photosymbioses |journal=Biological Reviews |language=en |volume=93 |issue=4 |pages=2006–2020 |doi=10.1111/brv.12430 |pmid=29808579 |issn=1464-7931|doi-access=free }} Tropical marine bivalves in the Cardiidae family form a symbiotic relationship with the dinoflagellate Symbiodinium.{{Cite journal |last=HERNAWAN |first=UDHI EKO |date=2008-12-06 |title=REVIEW: Symbiosis between the Giant Clams (Bivalvia: Cardiidae) and Zooxanthellae (Dinophyceae) |journal=Biodiversitas Journal of Biological Diversity |volume=9 |issue=1 |doi=10.13057/biodiv/d090112 |issn=2085-4722|doi-access=free }} This family boasts large organisms often referred to as giant clams and their large size is attributed to the establishment of these symbiotic relationships. Additionally, the Symbiodinium are hosted extracellularly, which is relatively rare.{{Cite journal |last1=Septiadi |first1=Angga |last2=Hernawan |first2=Hernawan |last3=Widiastuti |first3=Widiastuti |date=2019-11-10 |journal=Journal Sport Area |volume=4 |issue=2 |pages=285 |doi=10.25299/sportarea.2019.vol4(2).1803 |issn=2528-584X|doi-access=free }} The only known freshwater bivalve with a symbiotic relationship are in the genus Anodonta which hosts the chlorophyte Chlorella in the gills and mantle of the host.{{Cite journal |last=PARDY |first=R. L. |date=June 1980 |title=SYMBIOTIC ALGAE AND¹⁴C INCORPORATION IN THE FRESHWATER CLAM,ANODONTA |url=http://dx.doi.org/10.2307/1540861 |journal=The Biological Bulletin |volume=158 |issue=3 |pages=349–355 |doi=10.2307/1540861 |jstor=1540861 |issn=0006-3185}} In bivalves, photosymbiosis is thought to have evolved twice, in the genus Anodonta and in the family Cardiidae.{{Cite journal |last=PARDY |first=R. L. |date=June 1980 |title=SYMBIOTIC ALGAE AND¹⁴C INCORPORATION IN THE FRESHWATER CLAM,ANODONTA |url=http://dx.doi.org/10.2307/1540861 |journal=The Biological Bulletin |volume=158 |issue=3 |pages=349–355 |doi=10.2307/1540861 |jstor=1540861 |issn=0006-3185}} However, how it has evolved in Cardiidae could have occurred through different gains or losses in the family.{{Cite journal |last1=Maruyama |first1=T. |last2=Ishikura |first2=M. |last3=Yamazaki |first3=S. |last4=Kanai |first4=S. |date=August 1998 |title=Molecular Phylogeny of Zooxanthellate Bivalves |url=http://dx.doi.org/10.2307/1542777 |journal=The Biological Bulletin |volume=195 |issue=1 |pages=70–77 |doi=10.2307/1542777 |jstor=1542777 |pmid=9739550 |issn=0006-3185}}

In gastropods, photosymbiosis can be found in several genera.

The species Strombus gigas hosts Symbiodinium which is acquired during the larval stage, at which point it is a mutualistic relationship.{{Citation |last=Drewett |first=Peter L. |title=Strombus gigas (Queen Conch) |date=2014-03-04 |encyclopedia=Encyclopedia of Caribbean Archaeology |pages=329–330 |url=http://dx.doi.org/10.2307/j.ctvx1hst1.172 |access-date=2024-05-08 |publisher=University Press of Florida|doi=10.2307/j.ctvx1hst1.172 |url-access=subscription }} However, during the adult stage, Symbiodinium becomes parasitic as the shell prevents photosynthesis.{{Cite journal |last1=Banaszak |first1=Anastazia T. |last2=García Ramos |first2=Maribel |last3=Goulet |first3=Tamar L. |date=November 2013 |title=The symbiosis between the gastropod Strombus gigas and the dinoflagellate Symbiodinium: An ontogenic journey from mutualism to parasitism |url=http://dx.doi.org/10.1016/j.jembe.2013.10.027 |journal=Journal of Experimental Marine Biology and Ecology |volume=449 |pages=358–365 |doi=10.1016/j.jembe.2013.10.027 |bibcode=2013JEMBE.449..358B |issn=0022-0981|url-access=subscription }}

Another group of gastropods, heterobranch sea slugs, have two different systems for symbiosis. The first, Nudibranchia, acquire their symbionts through feeding on cnidarian prey that are in symbiotic relationships.{{Cite journal |last=BURGHARDT |first=I |date=2008-03-27 |title=Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analyses of long-term retention |url=http://dx.doi.org/10.1016/j.ode.2007.01.001 |journal=Organisms Diversity & Evolution |volume=8 |issue=1 |pages=66–76 |doi=10.1016/j.ode.2007.01.001 |bibcode=2008ODivE...8...66B |issn=1439-6092}} In Nudibranchs, photosymbiosis has evolved twice, in Melibe and Aeolidida.{{Cite journal |last1=Melo Clavijo |first1=Jenny |last2=Donath |first2=Alexander |last3=Serôdio |first3=João |last4=Christa |first4=Gregor |date=November 2018 |title=Polymorphic adaptations in metazoans to establish and maintain photosymbioses |journal=Biological Reviews |language=en |volume=93 |issue=4 |pages=2006–2020 |doi=10.1111/brv.12430 |pmid=29808579 |issn=1464-7931|doi-access=free }} In Aeolidida it is likely there have been several gains and losses of photosymbiosis as most genera include both photosymbiotic and non-photosymbiotic species.{{Cite journal |last1=Melo Clavijo |first1=Jenny |last2=Donath |first2=Alexander |last3=Serôdio |first3=João |last4=Christa |first4=Gregor |date=November 2018 |title=Polymorphic adaptations in metazoans to establish and maintain photosymbioses |journal=Biological Reviews |language=en |volume=93 |issue=4 |pages=2006–2020 |doi=10.1111/brv.12430 |pmid=29808579 |issn=1464-7931|doi-access=free }} The second, Sacoglossa, removes chloroplasts from macroalgae when feeding and sequesters them into their digestive tract at which point they are called kleptoplasts.{{Cite journal |last1=Händeler |first1=Katharina |last2=Grzymbowski |first2=Yvonne P |last3=Krug |first3=Patrick J |last4=Wägele |first4=Heike |date=2009 |title=Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life |journal=Frontiers in Zoology |volume=6 |issue=1 |pages=28 |doi=10.1186/1742-9994-6-28 |doi-access=free |pmid=19951407 |issn=1742-9994|pmc=2790442 }} Whether these kleptoplasts maintain their photosynthetic capabilities depends on the host species ability to digest them properly.{{Cite journal |last1=Christa |first1=Gregor |last2=Gould |first2=Sven B. |last3=Franken |first3=Johanna |last4=Vleugels |first4=Manja |last5=Karmeinski |first5=Dario |last6=Händeler |first6=Katharina |last7=Martin |first7=William F. |last8=Wägele |first8=Heike |date=2014-05-23 |title=Functional kleptoplasty in a limapontioidean genus: phylogeny, food preferences and photosynthesis inCostasiella, with a focus onC. ocellifera(Gastropoda: Sacoglossa) |url=http://dx.doi.org/10.1093/mollus/eyu026 |journal=Journal of Molluscan Studies |volume=80 |issue=5 |pages=499–507 |doi=10.1093/mollus/eyu026 |issn=0260-1230}} In this group, functional kleptoplasy has been acquired twice, in Costasiellidae and Plakobranchacea.{{Cite journal |last1=Christa |first1=Gregor |last2=Gould |first2=Sven B. |last3=Franken |first3=Johanna |last4=Vleugels |first4=Manja |last5=Karmeinski |first5=Dario |last6=Händeler |first6=Katharina |last7=Martin |first7=William F. |last8=Wägele |first8=Heike |date=December 2014 |title=Functional kleptoplasty in a limapontioidean genus: phylogeny, food preferences and photosynthesis in Costasiella , with a focus on C. ocellifera (Gastropoda: Sacoglossa) |url=https://academic.oup.com/mollus/article-lookup/doi/10.1093/mollus/eyu026 |journal=Journal of Molluscan Studies |language=en |volume=80 |issue=5 |pages=499–507 |doi=10.1093/mollus/eyu026 |issn=0260-1230}}

Photosymbiosis is relatively uncommon in chordate species.{{Cite journal |last1=Melo Clavijo |first1=Jenny |last2=Donath |first2=Alexander |last3=Serôdio |first3=João |last4=Christa |first4=Gregor |date=November 2018 |title=Polymorphic adaptations in metazoans to establish and maintain photosymbioses |journal=Biological Reviews |language=en |volume=93 |issue=4 |pages=2006–2020 |doi=10.1111/brv.12430 |pmid=29808579 |issn=1464-7931|doi-access=free }} One such example of photosymbiosis is in ascidians, the sea squirts. In the genus Didemnidae, 30 species establish symbiotic relationships.{{Cite journal |last=Hirose |first=Euichi |date=2014-04-15 |title=Ascidian photosymbiosis: Diversity of cyanobacterial transmission during embryogenesis |url=http://dx.doi.org/10.1002/dvg.22778 |journal=Genesis |volume=53 |issue=1 |pages=121–131 |doi=10.1002/dvg.22778 |pmid=24700539 |issn=1526-954X}} The photosynthetic ascidians are associated with cyanobacteria in the genus of Prochloron as well as, in some cases, the species Synechocystis trididemni.{{Cite journal |last=Hirose |first=Euichi |date=2014-04-15 |title=Ascidian photosymbiosis: Diversity of cyanobacterial transmission during embryogenesis |url=http://dx.doi.org/10.1002/dvg.22778 |journal=Genesis |volume=53 |issue=1 |pages=121–131 |doi=10.1002/dvg.22778 |pmid=24700539 |issn=1526-954X}} The 30 species with a symbiotic relationship span four genera where the congeners (species within the same genus) are primarily non-symbiotic, suggesting multiple origins of photosymbiosis in ascidians.{{Cite journal |last1=Yokobori |first1=Shin-ichi |last2=Kurabayashi |first2=Atsushi |last3=Neilan |first3=Brett A. |last4=Maruyama |first4=Tadashi |last5=Hirose |first5=Euichi |date=July 2006 |title=Multiple origins of the ascidian-Prochloron symbiosis: Molecular phylogeny of photosymbiotic and non-symbiotic colonial ascidians inferred from 18S rDNA sequences |url=http://dx.doi.org/10.1016/j.ympev.2005.11.025 |journal=Molecular Phylogenetics and Evolution |volume=40 |issue=1 |pages=8–19 |doi=10.1016/j.ympev.2005.11.025 |pmid=16531073 |bibcode=2006MolPE..40....8Y |issn=1055-7903|url-access=subscription }}

In addition to sea squirts, embryos of some amphibian species (Ambystoma maculatum, Ambystoma gracile, Ambystoma jeffersonium, Ambystoma trigrinum, Hynobius nigrescens, Lithobates sylvaticus, and Lithobates aurora) form symbiotic relationships with the green alga in the genus of Oophila.{{Cite journal |last=Gilbert |first=Perry W. |date=July 1944 |title=The Alga-Egg Relationship in Ambystoma Maculatum, A Case of Symbiosis |url=http://dx.doi.org/10.2307/1931284 |journal=Ecology |volume=25 |issue=3 |pages=366–369 |doi=10.2307/1931284 |jstor=1931284 |bibcode=1944Ecol...25..366G |issn=0012-9658|url-access=subscription }}{{Cite journal |last1=Muto |first1=Kiyoaki |last2=Nishikawa |first2=Kanto |last3=Kamikawa |first3=Ryoma |last4=Miyashita |first4=Hideaki |date=April 2017 |title=Symbiotic green algae in eggs of Hynobius nigrescens, an amphibian endemic to Japan |url=http://dx.doi.org/10.1111/pre.12173 |journal=Phycological Research |volume=65 |issue=2 |pages=171–174 |doi=10.1111/pre.12173 |bibcode=2017PhycR..65..171M |issn=1322-0829|url-access=subscription }}{{Cite journal |last1=Kerney |first1=Ryan |last2=Kim |first2=Eunsoo |last3=Hangarter |first3=Roger P. |last4=Heiss |first4=Aaron A. |last5=Bishop |first5=Cory D. |last6=Hall |first6=Brian K. |date=2011-04-04 |title=Intracellular invasion of green algae in a salamander host |journal=Proceedings of the National Academy of Sciences |volume=108 |issue=16 |pages=6497–6502 |doi=10.1073/pnas.1018259108 |doi-access=free |pmid=21464324 |pmc=3080989 |bibcode=2011PNAS..108.6497K |issn=0027-8424}} This algae is present in the egg masses of the species, causing them to appear green and providing oxygen and carbohydrates to the embryos.{{Cite journal |last1=Marco |first1=Adolfo |last2=Blaustein |first2=Andrew R. |date=December 2000 |title=Symbiosis with Green Algae Affects Survival and Growth of Northwestern Salamander Embryos |url=https://www.jstor.org/stable/1565283 |journal=Journal of Herpetology |volume=34 |issue=4 |pages=617 |doi=10.2307/1565283|jstor=1565283 |hdl=10261/48328 |hdl-access=free }} Similarly, little is known about the evolution of symbiosis in amphibians, but there appears to be multiple origins.

Photosymbiosis has evolved multiple times in the protist taxa Ciliophora, Foraminifera, Radiolaria, Dinoflagellata, and diatoms.{{Citation |last1=Decelle |first1=Johan |title=Photosymbiosis in Marine Planktonic Protists |date=2015 |work=Marine Protists |pages=465–500 |url=http://dx.doi.org/10.1007/978-4-431-55130-0_19 |access-date=2024-05-08 |place=Tokyo |publisher=Springer Japan |isbn=978-4-431-55129-4 |last2=Colin |first2=Sébastien |last3=Foster |first3=Rachel A.|doi=10.1007/978-4-431-55130-0_19 |url-access=subscription }} Foraminifera and Radiolaria are planktonic taxa that serve as primary producers in open ocean communities.{{Cite journal |last=Decelle |first=Johan |date=2013-07-30 |title=New perspectives on the functioning and evolution of photosymbiosis in plankton: Mutualism or parasitism? |journal=Communicative & Integrative Biology |language=en |volume=6 |issue=4 |pages=e24560 |doi=10.4161/cib.24560 |issn=1942-0889 |pmc=3742057 |pmid=23986805}} Photosynthetic plankton species associate with the symbiotes of dinoflagellates, diatoms, rhodophytes, chlorophytes, and cyanophytes that can be transferred both vertically and horizontally.{{Cite journal |last1=Fay |first1=S. A. |last2=Weber |first2=M. X. |last3=Lipps |first3=J. H. |date=2009-06-05 |title=The distribution of Symbiodinium diversity within individual host foraminifera |journal=Coral Reefs |volume=28 |issue=3 |pages=717–726 |doi=10.1007/s00338-009-0511-y |bibcode=2009CorRe..28..717F |issn=0722-4028|doi-access=free }} In Foraminifera, benthic species will either have a symbiotic relationship with Symbiodinium or retain the chloroplasts present in algal prey species.{{Citation |last1=Decelle |first1=Johan |title=Photosymbiosis in Marine Planktonic Protists |date=2015 |work=Marine Protists |pages=465–500 |url=http://dx.doi.org/10.1007/978-4-431-55130-0_19 |access-date=2024-05-08 |place=Tokyo |publisher=Springer Japan |isbn=978-4-431-55129-4 |last2=Colin |first2=Sébastien |last3=Foster |first3=Rachel A.|doi=10.1007/978-4-431-55130-0_19 |url-access=subscription }} The planktonic species of Foraminifera associate primarily with Pelagodinium.{{Citation |last1=Decelle |first1=Johan |title=Photosymbiosis in Marine Planktonic Protists |date=2015 |work=Marine Protists |pages=465–500 |url=http://dx.doi.org/10.1007/978-4-431-55130-0_19 |access-date=2024-05-08 |place=Tokyo |publisher=Springer Japan |isbn=978-4-431-55129-4 |last2=Colin |first2=Sébastien |last3=Foster |first3=Rachel A.|doi=10.1007/978-4-431-55130-0_19 |url-access=subscription }} These species are often considered indicator species due to their bleaching in response to environmental stressors.{{Cite journal |last1=Hallock |first1=Pamela |last2=Williams |first2=D. E |last3=Fisher |first3=E. M |last4=Toler |first4=S. K |date=2006-01-01 |title=Bleaching in foraminifera with algal symbionts: implications for reef monitoring and risk assessment |journal=Anuário do Instituto de Geociências |volume=29 |issue=1 |pages=108–128 |doi=10.11137/2006_1_108-128 |issn=1982-3908|doi-access=free }} In the Radiolarian group Acantharia, photosynthetic species inhabit surface waters whereas non-photosynthetic species inhabit deeper waters. Photosynthetic Acantharia are associated with similar microalgae as the Foraminifera groups, but were also found to be associated with Phaeocystis, Heterocapsa, Scrippsiella, and Azadinium which were not previously known to be involved in photosynthetic relationships.{{Cite journal |last=Decelle |first=Johan |date=2013-07-30 |title=New perspectives on the functioning and evolution of photosymbiosis in plankton: Mutualism or parasitism? |journal=Communicative & Integrative Biology |language=en |volume=6 |issue=4 |pages=e24560 |doi=10.4161/cib.24560 |pmid=23986805 |pmc=3742057 |issn=1942-0889}} In addition, several of the species present in symbiotic relationships with Acantharia were oftentimes identical to the free-living species, suggesting horizontal transfer of symbiotes.{{Cite journal |last=Decelle |first=Johan |date=2013-07-30 |title=New perspectives on the functioning and evolution of photosymbiosis in plankton: Mutualism or parasitism? |journal=Communicative & Integrative Biology |language=en |volume=6 |issue=4 |pages=e24560 |doi=10.4161/cib.24560 |issn=1942-0889 |pmc=3742057 |pmid=23986805}} This provides insight into the evolutionary patterns responsible for these symbiotic relationships, suggesting that the selection for symbiosis is relatively weak and symbiosis is likely a result of the adaptive capacity of the host plankton species.

• Holobiont

{{reflist}}

Category:Photosynthesis

Category:Symbiosis

Category:Ecology