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Cell Biology of Cnidarian-Dinoflagellate Symbiosis

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Cell Biology of Cnidarian-Dinoflagellate Symbiosis Cell Biology of Cnidarian-Dinoflagellate Symbiosis Simon K. Davy,a Denis Allemand,b and Virginia M. Weisc School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealanda; Centre Scientifique de Monaco, Monacob; and Department of Zoology, Oregon State University, Corvallis, Oregon, USAc INTRODUCTION ............................................................................................................................................229 RECOGNITION AND PHAGOCYTOSIS ......................................................................................................................231 Downloaded from Modern Fields of Genomics and Host-Microbe Interactions Have Caused a Paradigm Shift in the Study of Symbiosis Establishment ..................231 Mechanisms of Symbiosis Establishment ................................................................................................................232 Recognition............................................................................................................................................232 (i) Studies of recognition in green Hydra ............................................................................................................233 (ii) MAMP-PRR signaling in cnidarian-dinoflagellate associations ...................................................................................233 Algal entry into hosts ..................................................................................................................................234 Arrest of phagosomal maturation .....................................................................................................................235 Evidence of apoptosis and autophagy during recognition ............................................................................................235 Evidence of cell signaling processes in recognition ...................................................................................................236 REGULATION OF HOST-SYMBIONT BIOMASS: SYMBIONT EXPULSION, DEGRADATION, AND CELL CYCLE CONTROL..................................236 http://mmbr.asm.org/ Expulsion and Degradation of Excess Symbionts ........................................................................................................236 Symbiont expulsion ...................................................................................................................................237 Symbiont degradation.................................................................................................................................238 Regulation of Symbiont and Host Cell Growth and Proliferation.........................................................................................239 Studies of green Hydra.................................................................................................................................239 Studies of cnidarian-dinoflagellate symbiosis..........................................................................................................240 (i) Resource limitation ...............................................................................................................................240 (ii) Progression of the symbiont cell cycle...........................................................................................................240 (iii) Circadian rhythmicity of the symbiont cell cycle ................................................................................................241 (iv) Host cell division ................................................................................................................................241 METABOLIC EXCHANGE AND NUTRIENT TRAFFICKING ...................................................................................................242 on August 8, 2012 by Oregon State University Inorganic Carbon Acquisition and Fixation...............................................................................................................242 Translocation of Photosynthetic Products................................................................................................................244 How much photosynthetically fixed carbon is translocated?..........................................................................................244 In what forms is photosynthetically fixed carbon translocated? .......................................................................................244 (i) Identification of nutrient transporters at the host-symbiont interface............................................................................245 (ii) Metabolite profiling..............................................................................................................................246 What stimulates and controls the translocation of photosynthetically fixed carbon? .................................................................246 Fluxes of Nitrogen and Phosphorus ......................................................................................................................247 CALCIFICATION WITHIN A SYMBIOTIC ORGANISM........................................................................................................248 Coral Calcification ........................................................................................................................................248 The Calcification Process .................................................................................................................................248 Relationships between Symbiosis and Calcification .....................................................................................................249 Light-enhanced calcification ..........................................................................................................................249 (i) Alteration of the inorganic chemistry.............................................................................................................249 (ii) Production of organic molecules by symbiotic dinoflagellates ..................................................................................249 Light regulation of skeletal morphology...............................................................................................................250 CONCLUDING REMARKS AND FUTURE DIRECTIONS ......................................................................................................250 APPENDIX 1.................................................................................................................................................251 APPENDIX 2.................................................................................................................................................251 ACKNOWLEDGMENTS......................................................................................................................................252 REFERENCES ................................................................................................................................................252 INTRODUCTION (e.g., hard and soft corals, sea anemones, jellyfish, and hydrocor- als) and dinoflagellate algae of the genus Symbiodinium (com- ymbiosis, the living together of two or more organisms in a monly referred to as zooxanthellae). These dinoflagellates typi- Sclose, protracted relationship, ranges from mutualism, where cally reside within the cells of the host cnidarian’s gastrodermis both partners benefit from the association, to parasitism, where (i.e., the innermost tissue layer that borders the gastrovascular one partner benefits and the other suffers. Moreover, symbioses can shift along a continuum between these extremes, with, for example, some mutualisms becoming parasitic under certain en- vironmental conditions (363). Address correspondence to Simon K. Davy, [email protected]. Symbioses between invertebrates and photosynthetic partners Copyright © 2012, American Society for Microbiology. All Rights Reserved. are abundant in the marine environment, with the best known doi:10.1128/MMBR.05014-11 being the mutualism between members of the phylum Cnidaria June 2012 Volume 76 Number 2 Microbiology and Molecular Biology Reviews p. 229–261 mmbr.asm.org 229 Davy et al. cavity), where they are bound by a membrane complex consisting and whether or how corals and other symbiotic cnidarians might of a series of membranes of algal origin plus an outermost host- survive climate change and other environmental perturbations. derived membrane (184, 389); this entire entity is referred to as the Here we will review in detail what is currently known, and symbiosome. The dinoflagellates can be acquired by maternal in- indeed what is not, about the cell biology of cnidarian-dinoflagel- heritance (79) or, more commonly, anew with each generation late symbiosis, including its links to coral calcification. In doing from the surrounding seawater (12) when they must invade their so, we aim to refocus attention on fundamental cellular aspects host and form a functional partnership in order to persist. that have been somewhat neglected since the early to mid-1980s, The cnidarian-dinoflagellate symbiosis is found across tem- when a more ecological approach began to dominate. In particu- perate and subtropical latitudes (see, e.g., references 252 and 410), lar, the 1990s and early 2000s saw an explosion of research con- but has particular ecological significance on tropical coral reefs. cerning the diversity and ecological distribution of
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