Photosymbiosis

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Photosymbiosis is a type of symbiosis where one of the organisms is capable of photosynthesis. [1]

Examples of photosymbiosis
Caloplaca thallincola.jpg
Lichen Variospora thallincola growing on rock
Paramecium bursaria.jpg
A ciliate, Paramecium bursaria, with green zoochlorellae living inside it endosymbiotically
Mussa angulosa.jpg
Mussa angulosa coral
Tridacna derasa 1.jpg
Southern giant clam Tridacna derasa
Upside-down jellyfish (Cassiopea xamachana).jpg
Upside-down jellyfish Cassiopea xamachana

Examples of photosymbiotic relationships include those in lichens, plankton, ciliates, and many marine organisms including corals, fire corals, giant clams, and jellyfish. [2] [3] [4]

Photosymbiosis is important in the development, maintenance, and evolution of terrestrial and aquatic ecosystems, for example in biological soil crusts, soil formation, supporting highly diverse microbial populations in soil and water, and coral reef growth and maintenance. [5] [6]

Plagiomnium affine laminazellen.jpeg
Plagiomnium affine moss cells with visible chloroplasts—a type of plastid.

When one organism lives within another symbiotically it’s called endosymbiosis. Photosymbiotic relationships where microalgae and/or cyanobacteria live within a heterotrophic host organism, are believed to have led to eukaryotes acquiring photosynthesis and to the evolution of plants. [7] [8]

Occurrence

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 [9] . Recent work suggests that non-photosynthetic bacterial microbiomes associated with lichens may also have functional significance to lichens [10] . Most mycobiont partners derive from the ascomycetes, and the largest class of lichenized fungi is Lecanoromycetes [11] . The vast majority of lichens derive photobionts from Chlorophyta (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 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 [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, 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 [15] . However, it has been shown that photosymbiotes are acquired vertically (transmission from parent to offspring) and/or horizontally (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 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 [15] . The evolution of photosymbiosis in corals was likely critical for the global establishment of coral reefs [18] . Corals are likewise adapted to eject damaged photosymbionts that generate high levels of toxic reactive oxygen species, a process known as bleaching [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 basal bilaterians, photosymbiosis in marine or brackish systems is present only in the family Convolutidae [23] . In the group Acoela there is limited knowledge on the symbionts present, and they have been vaguely identified as zoochlorella or zooxanthella [24] [25] . 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 [26] [27] [28] [29] [30] [31] [32] [33] . In freshwater systems, photosymbiosis is present in platyhelminths belonging to the Rhabdocoela group [34] . In this group, members of the Provorticidae, Dalyeliidae, and Typhloplanidae 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 genus Chlorella [37] .

Photosymbiosis is taxonomically restricted in Mollusca [38] . Tropical marine bivalves in the Cardiidae family form a symbiotic relationship with the dinoflagellate Symbiodinium [39] . 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 [40] . 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 [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] .

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 [44] . However, during the adult stage, Symbiodinium becomes parasitic 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 on cnidarian prey that are in symbiotic relationships [46] . In Nudibranchs, photosymbiosis has evolved twice, in Melibe and Aeolidida [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, removes chloroplasts from macroalgae when feeding and sequesters them into their digestive tract at which point they are called kleptoplasts [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, in Costasiellidae and Plakobranchacea [51] .

Photosymbiosis is relatively uncommon in chordate species [52] . One such example of photosymbiosis is in ascidians, the sea squirts. In the genus Didemnidae , 30 species establish symbiotic relationships [53] . The photosynthetic ascidians are associated with cyanobacteria in the genus of Prochloron as well as, in some cases, the species Synechocystis trididemni [54] . The 30 species with a symbiotic relationship span four genera where the congeners are primarily non-symbiotic, suggesting multiple origins of photosymbiosis in ascidians [55] . 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 [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 taxa Ciliophora, Foraminifera, Radiolaria, Dinoflagellata, and diatoms [60] . Foraminifera and Radiolaria are planktonic taxa that serve as primary producers in open ocean communities [61] . Photosynthetic plankton species associate with the symbiotes of dinoflagellates, diatoms, rhodophytes, chlorophytes, and cyanophytes that can be transferred both vertically and horizontally [62] . In Foraminifera, benthic species will either have a symbiotic relationship with Symbiodinium or retain the chloroplasts present in algal prey species [63] . The planktonic species of Foraminifera associate primarily with Pelagodinium [64] . These species are often considered indicator species due to their bleaching in response to environmental stressors [65] . 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 [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.

Related Research Articles

<span class="mw-page-title-main">Acantharea</span> Class of single-celled organisms

The Acantharea (Acantharia) are a group of radiolarian protozoa, distinguished mainly by their strontium sulfate skeletons. Acantharians are heterotrophic marine microplankton that range in size from about 200 microns in diameter up to several millimeters. Some acantharians have photosynthetic endosymbionts and hence are considered mixotrophs.

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualistic relationship. Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

<span class="mw-page-title-main">Symbiosis</span> Close, long-term biological interaction between distinct organisms (usually species)

Symbiosis is any type of a close and long-term biological interaction between two biological organisms of different species, termed symbionts, be it mutualistic, commensalistic, or parasitic. In 1879, Heinrich Anton de Bary defined it as "the living together of unlike organisms". The term is sometimes used in the more restricted sense of a mutually beneficial interaction in which both symbionts contribute to each other's support.

<span class="mw-page-title-main">Zooplankton</span> Heterotrophic protistan or metazoan members of the plankton ecosystem

Zooplankton are the animal component of the planktonic community, having to consume other organisms to thrive. Plankton are aquatic organisms that are unable to swim effectively against currents. Consequently, they drift or are carried along by currents in the ocean, or by currents in seas, lakes or rivers.

<span class="mw-page-title-main">Dinoflagellate</span> Unicellular algae with two flagella

The dinoflagellates are a monophyletic group of single-celled eukaryotes constituting the phylum Dinoflagellata and are usually considered protists. Dinoflagellates are mostly marine plankton, but they also are common in freshwater habitats. Their populations vary with sea surface temperature, salinity, and depth. Many dinoflagellates are photosynthetic, but a large fraction of these are in fact mixotrophic, combining photosynthesis with ingestion of prey.

<span class="mw-page-title-main">Lichen</span> Symbiosis of fungi with algae or cyanobacteria

A lichen is a symbiosis of algae or cyanobacteria living among filaments of multiple fungi species, along with a yeast embedded in the cortex or "skin", in a mutualistic relationship. Lichens are important actors in nutrient cycling and act as producers which many higher trophic feeders feed on, such as reindeer, gastropods, nematodes, mites, and springtails. Lichens have properties different from those of their component organisms. They come in many colors, sizes, and forms and are sometimes plant-like, but are not plants. They may have tiny, leafless branches (fruticose); flat leaf-like structures (foliose); grow crust-like, adhering tightly to a surface (substrate) like a thick coat of paint (crustose); have a powder-like appearance (leprose); or other growth forms.

<span class="mw-page-title-main">Zooxanthellae</span> Dinoflagellates in symbiosis with coral, jellyfish and nudibranchs

Zooxanthellae is a colloquial term for single-celled dinoflagellates that are able to live in symbiosis with diverse marine invertebrates including demosponges, corals, jellyfish, and nudibranchs. Most known zooxanthellae are in the genus Symbiodinium, but some are known from the genus Amphidinium, and other taxa, as yet unidentified, may have similar endosymbiont affinities. The true Zooxanthella K.brandt is a mutualist of the radiolarian Collozoum inerme and systematically placed in Peridiniales. Another group of unicellular eukaryotes that partake in similar endosymbiotic relationships in both marine and freshwater habitats are green algae zoochlorellae.

<i>Symsagittifera roscoffensis</i> Species of flatworm-like animal

Symsagittifera roscoffensis, also called the Roscoff worm, the mint-sauce worm, or the shilly-shally worm, is a marine worm belonging to the phylum Xenacoelomorpha. The origin and nature of the green color of this worm stimulated the intrigued zoologists in the 1870's. It was discovered that the coloring resulted from the symbiosis between the animal and a green micro-algae, the species Tetraselmis convolutae, hosted under its epidermis. It is the photosynthetic activity of the micro-algae in hospite that provides the essential nutrients for the worm. This partnership is called photosymbiosis, from "photo", "light", and symbiosis "who lives with". These photosynthetic marine animals live in colonies on the tidal zone.

<i>Symbiodinium</i> Genus of dinoflagellates (algae)

Symbiodinium is a genus of dinoflagellates that encompasses the largest and most prevalent group of endosymbiotic dinoflagellates known and have photosymbiotic relationships with many species. These unicellular microalgae commonly reside in the endoderm of tropical cnidarians such as corals, sea anemones, and jellyfish, where the products of their photosynthetic processing are exchanged in the host for inorganic molecules. They are also harbored by various species of demosponges, flatworms, mollusks such as the giant clams, foraminifera (soritids), and some ciliates. Generally, these dinoflagellates enter the host cell through phagocytosis, persist as intracellular symbionts, reproduce, and disperse to the environment. The exception is in most mollusks, where these symbionts are intercellular. Cnidarians that are associated with Symbiodinium occur mostly in warm oligotrophic (nutrient-poor), marine environments where they are often the dominant constituents of benthic communities. These dinoflagellates are therefore among the most abundant eukaryotic microbes found in coral reef ecosystems.

Cyanobionts are cyanobacteria that live in symbiosis with a wide range of organisms such as terrestrial or aquatic plants; as well as, algal and fungal species. They can reside within extracellular or intracellular structures of the host. In order for a cyanobacterium to successfully form a symbiotic relationship, it must be able to exchange signals with the host, overcome defense mounted by the host, be capable of hormogonia formation, chemotaxis, heterocyst formation, as well as possess adequate resilience to reside in host tissue which may present extreme conditions, such as low oxygen levels, and/or acidic mucilage. The most well-known plant-associated cyanobionts belong to the genus Nostoc. With the ability to differentiate into several cell types that have various functions, members of the genus Nostoc have the morphological plasticity, flexibility and adaptability to adjust to a wide range of environmental conditions, contributing to its high capacity to form symbiotic relationships with other organisms. Several cyanobionts involved with fungi and marine organisms also belong to the genera Richelia, Calothrix, Synechocystis, Aphanocapsa and Anabaena, as well as the species Oscillatoria spongeliae. Although there are many documented symbioses between cyanobacteria and marine organisms, little is known about the nature of many of these symbioses. The possibility of discovering more novel symbiotic relationships is apparent from preliminary microscopic observations.

<span class="mw-page-title-main">Marine microorganisms</span> Any life form too small for the naked human eye to see that lives in a marine environment

Marine microorganisms are defined by their habitat as microorganisms living in a marine environment, that is, in the saltwater of a sea or ocean or the brackish water of a coastal estuary. A microorganism is any microscopic living organism or virus, which is invisibly small to the unaided human eye without magnification. Microorganisms are very diverse. They can be single-celled or multicellular and include bacteria, archaea, viruses, and most protozoa, as well as some fungi, algae, and animals, such as rotifers and copepods. Many macroscopic animals and plants have microscopic juvenile stages. Some microbiologists also classify viruses as microorganisms, but others consider these as non-living.

<i>Corculum cardissa</i> Species of bivalve

Corculum cardissa, the heart cockle, is a species of marine bivalve mollusc in the family Cardiidae. It is found in the Indo-Pacific region. It has a symbiotic relationship with dinoflagellates (zooxanthellae), which live within its tissues.

Durusdinium trenchii is an endosymbiotic dinoflagellate, a unicellular alga which commonly resides in the tissues of tropical corals. It has a greater tolerance to fluctuations in water temperatures than do other species in the genus. It was named for the marine biologist R. K. Trench.

<i>Phaeocystis</i> Genus of single-celled organisms

Phaeocystis is a genus of algae belonging to the Prymnesiophyte class and to the larger division of Haptophyta. It is a widespread marine phytoplankton and can function at a wide range of temperatures (eurythermal) and salinities (euryhaline). Members of this genus live in the open ocean, as well as in sea ice. It has a polymorphic life cycle, ranging from free-living cells to large colonies.

<i>Costasiella ocellifera</i> Species of gastropod

Costasiella ocellifera is a small (5–13 mm) species of sea slug, a shell-less marine gastropod mollusk in the family Costasiellidae. Costasiella ocellifera, and other members of the Costasiellidae family are often mistakenly classified as nudibranchs because they superficially resemble other species of that group, but they are actually a part of the Sacoglossa superorder of sea slugs, also known as the “sap-sucking sea slugs,” "crawling leaves" or the "solar-powered sea slugs." C. ocellifera was discovered by Simroth in 1895, and was initially classified as Doto ocellifera. The Brazilian species, Costasiella liliana, is a synonym of C. ocellifera.Costasiella ocellifera shows long-term retention of functional kleptoplasty.

Pelagodinium béii is a photosynthetic dinoflagellate that forms a symbiotic relationship with planktonic foraminifera.

<span class="mw-page-title-main">Marine protists</span> Protists that live in saltwater or brackish water

Marine protists are defined by their habitat as protists that live in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Life originated as marine single-celled prokaryotes and later evolved into more complex eukaryotes. Eukaryotes are the more developed life forms known as plants, animals, fungi and protists. Protists are the eukaryotes that cannot be classified as plants, fungi or animals. They are mostly single-celled and microscopic. The term protist came into use historically as a term of convenience for eukaryotes that cannot be strictly classified as plants, animals or fungi. They are not a part of modern cladistics because they are paraphyletic.

Robert Kent Trench was an American Biologist who was a professor at the University of California, Santa Barbara. His research considered corals and symbiotic algae, with a focus on the adaption of zooxanthellae. He was awarded the 1994 International Society of Endocytobiology Miescher-Ishida Prize.

<span class="mw-page-title-main">Mary Alice Coffroth</span> American marine biologist

Mary Alice Coffroth is an American marine biologist who is a professor at the State University of New York at Buffalo. She is known for her use of molecular tools to examine coral larval ecology, recruitment and cnidarian-dinoflagellate symbiosis.

<span class="mw-page-title-main">Symbiodiniaceae</span> Family of dinoflagellates (algae)

Symbiodiniaceae is a family of marine dinoflagellates notable for their symbiotic associations with reef-building corals, sea anemones, jellyfish, marine sponges, giant clams, acoel flatworms, and other marine invertebrates. Symbiotic Symbiodiniaceae are sometimes colloquially referred to as Zooxanthellae, though the latter term can be interpreted to include other families of symbiotic algae as well. While many Symbiodiniaceae species are endosymbionts, others are free living in the water column or sediment.

References

  1. ↑ "photosymbiosis". Oxford Reference.
  2. ↑ Gault J, Bentlage B, Huang D, Kerr A (2021). "Lineage-specific variation in the evolutionary stability of coral photosymbiosis". Science Advances. 7 (39): eabh4243. Bibcode:2021SciA....7.4243G. doi:10.1126/sciadv.abh4243. PMC   8457658 . PMID   34550731.
  3. ↑ Decelle, Johan (2013). "New perspectives on the functioning and evolution of photosymbiosis in plankton: Mutualism or parasitism?". Communicative & Integrative Biology. 6 (4): e24560. doi:10.4161/cib.24560. PMC   3742057 . PMID   23986805.
  4. ↑ Enrique-Navarro A, Huertas E, Flander-Putrle V, Bartual A, Navarro G, Ruiz J, Malej A, Prieto L. "Living Inside a Jellyfish: The Symbiosis Case Study of Host-Specialized Dinoflagellates, "Zooxanthellae", and the Scyphozoan Cotylorhiza tuberculata" . Retrieved 2023-06-18.
  5. ↑ Gault J, Bentlage B, Huang D, Kerr A (2021). "Lineage-specific variation in the evolutionary stability of coral photosymbiosis". Science Advances. 7 (39): eabh4243. Bibcode:2021SciA....7.4243G. doi:10.1126/sciadv.abh4243. PMC   8457658 . PMID   34550731.
  6. ↑ Stanley Jr G, Lipps J (2011). "Photosymbiosis: The Driving Force for Reef Success and Failure". The Paleontological Society Papers. 17: 33–59. doi:10.1017/S1089332600002436 . Retrieved 2023-06-18.
  7. ↑ Decelle, Johan (2013). "New perspectives on the functioning and evolution of photosymbiosis in plankton: Mutualism or parasitism?". Communicative & Integrative Biology. 6 (4): e24560. doi:10.4161/cib.24560. PMC   3742057 . PMID   23986805.
  8. ↑ Basic Biology (18 March 2016). "Bacteria".
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  10. ↑ Grube, Martin; Cernava, Tomislav; Soh, Jung; Fuchs, Stephan; Aschenbrenner, Ines; Lassek, Christian; Wegner, Uwe; Becher, Dörte; Riedel, Katharina; Sensen, Christoph W; Berg, Gabriele (2015-02-01). "Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics". The ISME Journal. 9 (2): 412–424. Bibcode:2015ISMEJ...9..412G. doi:10.1038/ismej.2014.138. ISSN   1751-7362. PMC   4303634 . PMID   25072413.
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  12. ↑ Yahr, Rebecca; Vilgalys, Rytas; DePriest, Paula T. (September 2006). "Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis". New Phytologist. 171 (4): 847–860. doi:10.1111/j.1469-8137.2006.01792.x. ISSN   0028-646X. PMID   16918555.
  13. ↑ Sanders, William B.; Masumoto, Hiroshi (September 2021). "Lichen algae: the photosynthetic partners in lichen symbioses". The Lichenologist. 53 (5): 347–393. doi:10.1017/S0024282921000335. ISSN   0024-2829.
  14. 1 2 Nelsen, Matthew P.; Lücking, Robert; Boyce, C. Kevin; Lumbsch, H. Thorsten; Ree, Richard H. (September 2020). "The macroevolutionary dynamics of symbiotic and phenotypic diversification in lichens". Proceedings of the National Academy of Sciences. 117 (35): 21495–21503. Bibcode:2020PNAS..11721495N. doi: 10.1073/pnas.2001913117 . ISSN   0027-8424. PMC   7474681 . PMID   32796103.
  15. 1 2 Melo Clavijo, Jenny; Donath, Alexander; Serôdio, João; Christa, Gregor (November 2018). "Polymorphic adaptations in metazoans to establish and maintain photosymbioses". Biological Reviews. 93 (4): 2006–2020. doi:10.1111/brv.12430. ISSN   1464-7931. PMID   29808579.
  16. ↑ de Oliveira, Bruno Francesco Rodrigues; Freitas-Silva, Jéssyca; Sánchez-Robinet, Claudia; Laport, Marinella Silva (December 2020). "Transmission of the sponge microbiome: moving towards a unified model". Environmental Microbiology Reports. 12 (6): 619–638. Bibcode:2020EnvMR..12..619D. doi:10.1111/1758-2229.12896. ISSN   1758-2229. PMID   33048474.
  17. ↑ Hudspith, Meggie; de Goeij, Jasper M; Streekstra, Mischa; Kornder, Niklas A; Bougoure, Jeremy; Guagliardo, Paul; Campana, Sara; van der Wel, Nicole N; Muyzer, Gerard; Rix, Laura (2022-06-02). "Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge". The ISME Journal. 16 (9): 2076–2086. Bibcode:2022ISMEJ..16.2076H. doi:10.1038/s41396-022-01254-3. ISSN   1751-7362. PMC   9381825 . PMID   35654830.
  18. ↑ Muscatine, Leonard; Goiran, Claire; Land, Lynton; Jaubert, Jean; Cuif, Jean-Pierre; Allemand, Denis (February 2005). "Stable isotopes (δ 13 C and δ 15 N) of organic matrix from coral skeleton". Proceedings of the National Academy of Sciences. 102 (5): 1525–1530. doi: 10.1073/pnas.0408921102 . ISSN   0027-8424. PMC   547863 . PMID   15671164.
  19. ↑ Weis, Virginia M. (2008-10-01). "Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis". Journal of Experimental Biology. 211 (19): 3059–3066. doi:10.1242/jeb.009597. ISSN   1477-9145. PMID   18805804.
  20. ↑ Padilla-Gamiño, Jacqueline L.; Pochon, Xavier; Bird, Christopher; Concepcion, Gregory T.; Gates, Ruth D. (2012-06-06). "From Parent to Gamete: Vertical Transmission of Symbiodinium (Dinophyceae) ITS2 Sequence Assemblages in the Reef Building Coral Montipora capitata". PLOS ONE. 7 (6): e38440. Bibcode:2012PLoSO...738440P. doi: 10.1371/journal.pone.0038440 . ISSN   1932-6203. PMC   3368852 . PMID   22701642.
  21. ↑ van Oppen, Madeleine J. H.; Medina, Mónica (2020-09-28). "Coral evolutionary responses to microbial symbioses". Philosophical Transactions of the Royal Society B: Biological Sciences. 375 (1808): 20190591. doi:10.1098/rstb.2019.0591. ISSN   0962-8436. PMC   7435167 . PMID   32772672.
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