Symbiosis is a general term that describes the situation in which different organisms live together in close association, including both mutualistic and parasitic relationships (Allaby, 2012). Mutualism must benefit both species populations. This review will focus on the mutualistic symbioses between cyanobacteria and a wide range of terrestrial and aquatic hosts.

Cyanobacteria are a large and varied group of photosynthetic bacteria, lacking a nucleus and membrane bound organelles. They are found on soil, on rocks, in both freshwater and marine environments, and in fossils dating back 3000Mya. They can be single-celled or filamentous, and may be colonial. While there are no chloroplasts, chlorophyll a is located on specialized membranes (thylakoids) within the cells (Allaby, 2012). Cyanobacteria form widely distributed mutualistic symbioses in diverse hosts: terrestrially in plants and fungi, and in marine environments with protists and invertebrates (Usher, et al. 2007). It has been recorded that cyanobacterial endosymbiosis with eukaryotes dates back to 2.1 billion years ago in an intercellular mutual relationship that led to the development of chloroplasts in the Kingdom Plantae (Lockhart et al 1992, Raven 2002). Mutualism with cyanobacteria provides numerous diverse benefits including allowing non-photosynthetic hosts to obtain energy from the sun, while some species provide UV protection, nitrogen fixation, and defensive toxin production (Usher, et al. 2007).
Authors Kayle M. Usher, Brigitta Bergman and John A. Raven in their article “Exploring Cyanobacterial Mutualisms” in the Annual Review of Ecology, Evolution, and Systematics, Vol. 38 (2007) provide an overview of cyanobacterial mutualism with aquatic and terrestrial eukaryotes, including benefits to the host, environmental range, modes of transmission, and patterns in their mutual evolution.
The intercellular symbiosis between host plant cells and cyanobacteria that formed chloroplasts is described as “one of the most important symbioses to have evolved (Usher, et al. 2007).” Plants have formed other obligate partnerships both intercellularly and intracellularly, the later in specialized structures such as bladders, cavities, root nodules and glands. Most plant-cyanobacterial symbioses grow in moist and wet habitats, similar to conditions of their ancient lineages (Osborne & Sprent 2002). These hosts include liverworts, hornworts, mosses, the water-fern Azolla, cycads, and the angiosperm Gunnera (Usher, et al. 2007). While plants do not necessarily need extra help photosynthesizing, they do benefit from nitrogen fixation, converting atmospheric nitrogen gas into a useable form.
Terrestrially, cyanobacteria also form symbiotic relationships with fungi. Lichens are a composite organism made up of a fungus (the mycobiont) living in symbiotic association with a phycobiont – an alga or cyanobacterium (Allaby, 2012). While most lichenized fungi contain algal symbionts, there are around 1000 species of ascomycete-cyanobacterial partnerships, referred to as cyanolichens (Rai & Bergman 2002). Evidence from recent discoveries of fossilized lichen suggest this symbiosis originated between 551 and 635Mya in shallow subtidal regions (Yuan et al. 2005).
There are no symbioses formed between cyanobacteria and terrestrial animals, it is thought that the energy provided by photosynthesis would be too small in comparison to energy needed for such exhaustive terrestrial processes, like locomotion (Usher, et al. 2007). Sessile marine invertebrates exert less metabolic activity by remaining holdfast to a substrate, and can therefore gain benefits from cyanobacterial partnerships. These include “a wide range of sponges, some ascidians, and a cnidarian (Larkum & Kühl 2005).” It is possible these symbionts provide benefits in addition to photosynthesis, including chemical defense, UV protection, and nitrogen fixation. Other marine mutualism include cyanobacterial partnerships with diatoms, dinoflagellates, and corals (Usher, et al. 2007).
Success in the evolution of these partnerships is measured by each species’ ability to use the by-products of one another (Genkai-Kato & Yamamura 1999). Usher et al. presents that “it is likely that in many cases mutualists are recognized and encouraged by the host.” Different hosts gain different benefits from their partnerships. Non-photosynthetic hosts, like marine invertebrates and lichen gain the ability to manufacture energy from the sun. While in partnerships with already photosynthetic organisms (plants, some corals, some cyanolichens, and diatoms) the amount of energy gained from the cyanobacteria photosynthesizing is minimal. Instead benefits are gained from their ability to fix nitrogen gas, allowing their hosts to grow in areas of low combined nitrogen, by converting it from the atmosphere (Usher, et al. 2007). Cyanobionts may also provide UV protection with the production of two types of sunscreen compounds (Shick & Dunlap 2002). Additionally cyanobionts can produce antibiotics, antifeedants, and powerful defense toxins (Borowitzka & Hindle 1999). These toxins provide chemical defense and protection to fungi, marine invertebrates and plant hosts (Usher, et al. 2007).
While mutualistic symbioses have independently evolved in a wide variety of organisms and biomes, Usher, Bergman and Raven argue that there are certain criteria that must be met for a successful mutualist symbiosis to occur. Among them include that the benefits provided by the cyanobacteria must be equal to or greater than the cost of hosting it and providing necessary elements (Fe, iron) for nitrogen fixation (Raven 2002). Another criteria dictating success is that the cyanobacteria must be in close contact for an association to evolve. Cyanobacteria are only metabolically active in moist or wet conditions, therefore symbiotic relationships will not be found in terrestrial habitats where soils dry out periodically or are too acidic (Usher, et al. 2007). And lastly, in organisms with multiple symbionts, there should be no conflict among other microbial symbionts. For example Azolla species have developed compartmentalized leaf cavities to separate their cyanobacterial and bacterial symbionts. Cyanobionts can be passed along to other members of a population in three ways: through ingestion (phagocytosis), vertical transmission (mother to offspring), or by horizontal transmission (from near by hosts in the same environment) (Usher, et al. 2007).
In review, the authors of “Exploring Cyanobacterial Mutualisms,” present a thorough and comprehensive introduction to cyanobacterial symbioses, provide a framework for recognizing and studying them, and encourage further research into the diversity of both hosts and symbionts. This research is important in understanding the evolution of the mutualistic associations, as well the evolution of the individual species. Future research into the benefits of these symbioses for survival, while concurrently studying the ages of the relationships, can evaluate how (and when) hosts evolve these mutualisms to adapt to their changing environment.

References:
Allaby M. (2012). Oxford Dictionary of Plant Sciences. Oxford: Oxford University Press, p. 136, 284 & 494.
Borowitzka M.A., Hindle R. (1999). Sponges symbiotic with algae or cyanobacteria in coral reefs. Assessment and Monitoring of Marine System. pp. 7 – 17. Teregganu, Kuala Teregganu: University Putra Malaysia.
Genkai-Kato M., Yamamura N. (1999). Evolution of mutualistic symbiosis without vertical transmission. Theor: Popul. Biol. 55:309-23
Larkum A.W.D., Kühl M. (2005). Chlorophyll d: the puzzle resolved. Trends Plant Sci. 10:355-57.
Lockhart P.J., Beanland T.J., Howe C.J., Larkum, A.W.D. (1992) Sequence of Prochloron didemni atpBE and the inference of chloroplast origins. Proc. Natl. Acad. Sci. USA 89:2742-46.
Osborne B.A., Sprent J.I. (2002). Ecology of the Nostoc-Gunnera symbioses. Biol. Environ. Prog. R. Ir. Acad. pp. 233-51.
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Raven J.A. (2002) The evolution of cyanobacterial symbiosis. Biol. Environ. Prog. R. Ir. Acad. 102B:3-6.
Shick J.M., Dunlap W.C. (2002). Mycosporine-like amino acids and related gadusols: Biosynthesis, accumulation and UV-protective functions in aquatic organisms. Annu. Rev. Physiol. 64:223-62.
*Usher K.M., Bergman B., Raven J.A. (2007). Exploring Cyanobacterial Mutualisms. Annual Review of Ecology, Evolution and Systematics. pp.255-272.
Yuan X., Xiao S., Taylor T.N. (2005). Lichen-like symbioses 600 mya. Science 308:1017-20.