Lichens represent an association between one or morefungal mycobionts and one or more photosyntheticalgal or cyanobacterial photobionts. The mycobiont provides protection from predation anddesiccation, while the photobiont provides energy in the form of fixed carbon. Cyanobacterial partners are also capable offixing nitrogen for the fungal partner.[9] Recent work suggests that non-photosynthetic bacterialmicrobiomes associated with lichens may also have functional significance to lichens.[10]
Most mycobiont partners derive from theascomycetes, and the largest class of lichenized fungi isLecanoromycetes.[11] The vast majority of lichens derive photobionts fromChlorophyta (green algae).[9] 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 ofreactive oxygen species (ROS), the conversion of sugars topolypols that help withstand dedication, and the downregulation of fungalvirulence. However, it is still unclear whether these are derived or ancestral traits.[9]
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.[12][13] 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.[11][14] Loss of lichenization has likely led to the coexistence of non-lichenized fungi and lichenized fungi in lichens.[14]
Sponges (phylum Porifera) have a large diversity of photosymbiote associations. Photosymbiosis is found in four classes of Porifera (Demospongiae,Hexactinellida,Homoscleromorpha, andCalcarea), 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 ofgenomic data.[15] However, it has been shown that photosymbiotes are acquiredvertically (transmission from parent to offspring) and/orhorizontally (acquired from the environment).[16] Photosymbiotes can supply up to half of the host sponge’s respiratory demands and can support sponges during times of nutrient stress.[17]
Members of certain classes in phylumCnidaria are known for photosymbiotic partnerships. Members of corals (ClassAnthozoa) in the ordersHexacorallia andOctocorallia form well-characterized partnerships with the dinoflagellate genusSymbiodinium. Some jellyfish (classScyphozoa) in the genusCassiopea (upside-down jellyfish) also possess Symbiodinium. Certain species in the genusHydra (classHydrozoa) also harbor green algae and form a stable photosymbiosis.[15]
The evolution of photosymbiosis in corals was likely critical for the global establishment ofcoral reefs.[18] Corals are likewise adapted to eject damaged photosymbionts that generate high levels of toxic reactive oxygen species, a process known asbleaching.[19] 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,[20] while other species acquire environmental dinoflagellates as newly-released eggs.[21] Since algae are not preserved in the coral fossil record, understanding the evolutionary history of the symbiosis is difficult.[22]
In freshwater systems, photosymbiosis is present inplatyhelminths belonging to theRhabdocoela group.[34] In this group, members of theProvorticidae,Dalyeliidae, andTyphloplanidae families are symbiotic.[35] Members of Provorticidae likely feed on diatoms and retain their symbionts.[36] Typhloplanidae have symbiotic relationships with the chlorophytes in the genusChlorella.[37]
Photosymbiosis is taxonomically restricted inMollusca.[38] Tropical marinebivalves in theCardiidae family form a symbiotic relationship with the dinoflagellateSymbiodinium.[39] This family boasts large organisms often referred to asgiant clams and their large size is attributed to the establishment of these symbiotic relationships. Additionally, the Symbiodinium are hosted extracellularly, which is relatively rare.[40] The only known freshwater bivalve with a symbiotic relationship are in the genusAnodonta which hosts the chlorophyte Chlorella in the gills andmantle of the host.[41] In bivalves, photosymbiosis is thought to have evolved twice, in the genus Anodonta and in the family Cardiidae.[42] However, how it has evolved in Cardiidae could have occurred through different gains or losses in the family.[43]
Ingastropods, photosymbiosis can be found in several genera.
The speciesStrombus gigas hostsSymbiodinium which is acquired during the larval stage, at which point it is amutualistic relationship.[44] However, during the adult stage, Symbiodinium becomesparasitic as the shell prevents photosynthesis.[45]
Another group of gastropods,heterobranch sea slugs, have two different systems for symbiosis. The first,Nudibranchia, acquire their symbionts through feeding oncnidarian prey that are in symbiotic relationships.[46] In Nudibranchs, photosymbiosis has evolved twice, inMelibe andAeolidida.[47] In Aeolidida it is likely there have been several gains and losses of photosymbiosis as most genera include both photosymbiotic and non-photosymbiotic species.[48] The second,Sacoglossa, removeschloroplasts from macroalgae when feeding and sequesters them into their digestive tract at which point they are calledkleptoplasts.[49] Whether these kleptoplasts maintain their photosynthetic capabilities depends on the host species ability to digest them properly.[50] In this group, functional kleptoplasy has been acquired twice, inCostasiellidae andPlakobranchacea.[51]
Photosymbiosis is relatively uncommon inchordate species.[52] One such example of photosymbiosis is inascidians, the sea squirts. In the genusDidemnidae, 30 species establish symbiotic relationships.[53] The photosynthetic ascidians are associated withcyanobacteria in the genus ofProchloron as well as, in some cases, the speciesSynechocystis trididemni.[54] The 30 species with a symbiotic relationship span four genera where thecongeners (species within the same genus) are primarily non-symbiotic, suggesting multiple origins of photosymbiosis in ascidians.[55]
In addition to sea squirts, embryos of someamphibian species (Ambystoma maculatum,Ambystoma gracile, Ambystoma jeffersonium,Ambystoma trigrinum,Hynobius nigrescens,Lithobates sylvaticus, and Lithobates aurora) form symbiotic relationships with thegreen alga in the genus of Oophila.[56][57][58] This algae is present in the egg masses of the species, causing them to appear green and providing oxygen and carbohydrates to the embryos.[59] 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 taxaCiliophora,Foraminifera,Radiolaria,Dinoflagellata, anddiatoms.[60] Foraminifera and Radiolaria areplanktonic taxa that serve asprimary producers in open ocean communities.[61] Photosynthetic plankton species associate with the symbiotes of dinoflagellates, diatoms,rhodophytes,chlorophytes, andcyanophytes that can be transferred bothvertically andhorizontally.[62] In Foraminifera,benthic species will either have a symbiotic relationship withSymbiodinium or retain the chloroplasts present in algal prey species.[63] The planktonic species of Foraminifera associate primarily withPelagodinium.[64] These species are often considered indicator species due to their bleaching in response to environmental stressors.[65] In the Radiolarian groupAcantharia, 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 withPhaeocystis,Heterocapsa, Scrippsiella, andAzadinium which were not previously known to be involved in photosynthetic relationships.[66] 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.[67] 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.
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