118 Marine Symbioses: Metazoans and Microbes protective compounds (Turnbaugh et al., 2007), so it is important to remember that metazoans utilize symbiotic associations as a way to expand our physiological and metabolic capabilities In general, metazoans are quite limited in their capacity to process or obtain nutrients, and they rely on the diverse metabolisms of microbes to supplement their native capabilities The symbioses discussed in this article highlight some of those traits and describe how microbes have been coopted to function in metazoan hosts, creating a unique niche for both organisms in the marine environment Nutrient-Exchange Mutualisms Photosynthetic Symbioses The phenomenon of photosynthesis evolved once, originating in cyanobacteria (Cavalier-Smith, 2006) Today, a significant amount of global photosynthesis is still performed by cyanobacteria in the oceans, with land plants and algae contributing to the rest of the photosynthesis on this planet If photosynthesis evolved only once in cyanobacteria, where did plant and algal chloroplasts originate? In 1905, Constantin Mereschkowsky first presented the concept that chloroplasts are derived from an ancient endosymbiotic event that combined cyanobacteria with a eukaryotic host (translated in Martin and Kowallik, 1999) This theory was later strengthened and expanded by Lynn Margulis in 1967 (as L Sagan), with her presentation of cytological, biochemical, and paleontological evidence for a generalized symbiosis theory (Sagan, 1967) and by the discovery that chloroplasts contain DNA related to cyanobacteria (Bonen and Doolittle, 1975; Ris and Plaut, 1962; Zablen et al., 1975) Aside from land plants and lichens (fungi in association with photosymbionts), all multicellular organisms with photosynthetic symbionts are found in aquatic environments The marine environment contains a variety of ‘‘photosynthetic animals,’’ or metazoans in association with photosynthetic microbes such as cyanobacteria However, most of the photosynthetic animal hosts in the marine environment are actually secondary mutualisms – situations in which a primary mutualism such as a eukaryotic alga containing chloroplast organelles is incorporated into a secondary host These secondarily photosynthetic associations are often found thriving under low nutrient conditions that typically limit food abundance (Johnson, 2011; Vaughn et al., 2010) The photosynthetic symbiont uses sunlight to fix carbon dioxide (CO2) into organic carbon, much of which is directly translocated to the host to supplement feeding In return, the host provides a stable, high light environment with a constant supply of CO2 and nutrients such as nitrogen and phosphorus Several host examples highlighted in this article are cnidarians, such as corals and anemones, bivalves like the giant clam, and the sea slug (Elysia spp.), which has a unique kleptoplastic nature (Figure 3) Cnidarians have a relatively simple body plan comprised of two cell layers: an outer epidermis, which is a central acellular lay of mesoglea, and an inner gastrodermis that lines the digestive cavity and houses the intracellular endosymbionts (Figure 3(a)) Symbiont transmission between generations can be vertical or horizontal, depending on the host species Hosts that employ vertical transmission typically transmit symbionts in egg cells that become fertilized to produce offspring or, in the case of brooding species, may transfer symbionts to offspring while they are still within the parent colony (Figure 2(b)) Horizontal transmission is established through feeding: the host’s gastrodermal cells phagocytose the symbionts, and the symbionts survive by resisting digestion through mechanisms not yet understood For reef-building corals, the symbiosis is considered obligate However, some hosts, such as the sea anemone Aiptasia (Figure 3(b)), and some strains of the symbiotic algae, can be found free-living Regardless of lifestyle, symbiotic cnidarians are only found in association with dinoflagellates in the genus Symbiodinium, which is described later in this section Corals (animal host and algal symbiont) living in warm, shallow waters have a unique role in the marine environment They create the biological and structural foundation for the most diverse marine ecosystem on the planet: coral reefs The reef structure is built by coral polyps, clonal individuals resembling anemones, that deposit a thin layer of calcium carbonate, layer by layer, generation after generation, for decades or even centuries (Figure 3(c)) Since corals typically live in low-nutrient waters, the nutritional supplement provided by their photosynthetic symbionts significantly enhances calcification and therefore growth of the colony The coral structure provides habitat for many of the diverse organisms that live on coral reefs Some corals with branching morphology show rapid growth, laying down 10–20 cm of skeleton per year, whereas corals with a more uniform, massive structure are estimated to add only 0.5–1 cm of growth per year (Figure 3(d)) Reef building is a dynamic process Even as corals build the reef, wave motion and biological perturbation continuously degrade it The reefs we are familiar with today have been around for thousands of years; however, changing environmental conditions on a global scale (increasing sea surface temperatures and ocean acidification) and on local scales (sedimentation and eutrophication from coastal runoff) are undermining the corals efforts to maintain the structure of the reef, and these important yet fragile ecosystems may eventually be lost in many places around the globe Giant clams are the largest bivalves in the world, reaching up to 120 cm in length and weighing more than 200 kg (Figure 3(e)) They are found in association with coral reefs in the South Pacific and Indian oceans They also host Symbiodinium dinoflagellates as symbionts, with symbionts being acquired by host larvae during feeding Symbionts that successfully avoid digestion are housed extracellularly in a tubular extension of the stomach that branches out into the mantle cavity This structure is designed to provide the symbionts with ample light for photosynthesis and also creates the unique patterns observed in the clam’s mantle tissue For the clam, this is an obligate association, with up to 95% of the photosynthetically fixed carbon being translocated to meet the host’s metabolic requirements Symbiodinium, the genus of dinoflagellate symbionts found in cnidarians and giant clams, was originally thought to be a single species, Symbiodinium microadriaticum Freudenthal (Freudenthal, 1962) Advances in genetic techniques have revealed at least nine different lineages within Symbiodinium