!"#$"%& Virus–host interactions and their roles in coral reef health and disease Rebecca Vega Thurber1, Jérôme P. Payet1,2, Andrew R. Thurber1,2 and Adrienne M. S. Correa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cycling. Last, we outline how marine viruses are an integral part of the reef system and suggest $4&$($4-(01.,/-1'-(+.(80%/#-#(+1(%--.(./1'$0+1(0#(&1(-##-1$0&,('+>3+1-1$(+.($4-#-(:,+"&,,9( 0>3+%$&1$(-180%+1>-1$#; To p - d ow n e f f e c t s Viruses infect all cellular life, including bacteria and evidence that macroorganisms play important parts in The ecological concept that eukaryotes, and contain ~200 megatonnes of carbon the dynamics of viroplankton; for example, sponges can organismal growth and globally1 — thus, they are integral parts of marine eco- filter and consume viruses6,7. abundance are primarily systems2,3. Since the discovery of the remarkably high This Review summarizes our current knowledge of regulated by predation (for example, grazing and viral abundance and widespread occurrence of viruses in viruses in tropical coral reef ecosystems. Drawing on 4 infection) as opposed to sea water in the 1980s , ocean viruses have been inten- marine virology and coral reef biology research, we dis- resource limitation. sively studied, with research focusing on the effects of cuss when and how viral consortia shift on reefs and how viruses on biogeochemical processes and ecosystem this may affect the health and function of coral reef eco- function, and their top-down effects on microbial food systems. We discuss the dynamics of coral reef virology webs (BOX 1). through the lens of coral reef decline, which has been a Most marine virology has focused on pelagic open- cause for increasing concern worldwide since the late ocean systems and temperate coastal seas, but the 1970s and is primarily driven by climate change, over- virology of coral reefs has started to gain attention only fishing and nutrient pollution8–10. To conclude, we high- during the past 15 years. Tropical shallow reef envi- light the interconnection between viral infection in reef ronments are coastal benthic habitats that, although hosts and concentrations of nutrients and community 1Department of Microbiology, constituting less than 0.5% of the ocean seabed, con- diversity in reef sea water. Oregon State University, tain approximately 25% of all marine species. These Corvallis, Oregon 97331, USA. diverse habitats are dominated by scleractinian (stony) !"#$%&'()$'##*$#%&+,+-#. 2 College of Earth, Ocean, corals and other sessile invertebrate organisms such Tropical coral reefs occur in nutrient-poor environ- and Atmospheric Science, as soft corals and sponges, in addition to macroalgae. ments, but they still form highly productive and diverse Oregon State University, 11,12 Corvallis, Oregon 97331, Importantly, stony corals build the foundation of the eco systems . This observation of an ecosystem with USA. reef and release large amounts of carbon, and perhaps high biodiversity and low nutrient input is known as 3 BioSciences Department, nitrogen, to the surrounding environment5. In the open Darwin’s paradox13. In healthy reefs, marine microbial Rice University, 6100 Main ocean, bacterio plankton and therefore phages dominate communities are the ‘solution’ to this apparent paradox: Street, Houston, Texas 14 77005, USA. research efforts, whereas on coral reefs virologists often marine phyto plankton in the water column together examine eukaryotic viruses and phages that are associated with dino flagellate endosymbiotic algae in the genus Correspondence to R.V.T. Symbiodinium and A.M.S.C.Rebecca.Vega- with benthic stony corals and their inhabitants, as well , which leak up to 95% of their photo- 15 [email protected]; as the viruses that are associated with the water column synthesized sugars into coral tissues , provide their [email protected] that bathes these macroorganisms. Little is known about habitats and hosts with the energy that is required to doi:10.1038/nrmicro.2016.176 viral interaction or exchange between the benthic zone construct substantial reef frameworks. Corals also har- Published online 16 Jan 2017 and the water column in reef systems. However, there is bour a diversity of symbiotic bacteria and viruses in their !"#$%&'%&()&*+','"#$%&'#&(&)*! 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