Zooxanthellae harvested by ciliates associated with brown band syndrome of corals remain photosynthetically competent

Applied and Environmental Microbiology

Volumn 73, Issue 6, 2007, Pages 1968-1975

  Ulstrup, Karin E ^a,b   Kühl, Michael ^c   Bourne, David G ^b  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL; FLUORESCENCE; PHOTOSYNTHESIS;

BROWN BAND SYNDROME; MICROSCALE OXYGEN MEASUREMENTS; PHOTOSYSTEM II; RADIATION ABSORPTIVITY;

MICROBIOLOGY;

CHLOROPHYLL A;

CHLOROPHYLL; CILIATE; CORAL; LIGHT USE EFFICIENCY; PHOTOSYNTHESIS; SYMBIOSIS; ZOOXANTHELLA;

ACCLIMATIZATION; ALGA; ALGAL BLOOM; ARTICLE; BROWN BAND SYNDROME; CILIATE; CORAL; DIFFUSION; DINOFLAGELLATE; FLUORESCENCE; GRAZING; LIGHT ABSORPTION; NONHUMAN; PHOTOSYNTHESIS; PHOTOSYSTEM II; RADIATION ABSORPTION; SYMBIODINIUM; SYMBIOSIS;

ANIMALS; ANTHOZOA; CHLOROPHYLL; CILIOPHORA; DINOFLAGELLIDA; ELECTRON TRANSPORT; IMAGE PROCESSING, COMPUTER-ASSISTED; LIGHT; MICROSCOPY, FLUORESCENCE; OXYGEN; PHOTOSYNTHESIS; SYMBIOSIS;

ANTHOZOA; CILIOPHORA; DINOPHYCEAE; SYMBIODINIUM;

EID: 33947386688     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02292-06     Document Type: Article

References (56)

1. Antonius, A. 1999. Halofolliculina corallasia, a new coral-killer ciliate on Indo-Pacific reefs. Coral Reefs 18:300.
2. Antonius, A, and D. Lipscomb. 2001. First protozoan coral-killer identified in the Indo-Pacific. Atoll Res. Bull. 493:1-21.
3. Bancroft, J. D., and A. Stevens. 1990. Theory and practice of histological techniques. Churchill Livingstone, Edinburgh, United Kingdom.
4. Berk, S. G., L. H. Parkes, and R. S. Ting. 1991. Photoadaptation alters the ingestion rate of Paramecium bursaria, a mixotrophic ciliate. Appl. Environ. Microbiol. 57:2312-2316.
5. Brown, B. E., M. D. A. Le Tissier, and J. C. Bythell. 1995. Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar. Biol. 122:655-663.
6. Cooney, R. P, O. Pantos, M. D. A. Le Tissier, M. R. Barer, A. G. O'Donnell, and J. C. Bythell. 2002. Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ. Microbiol. 4:401-413.
7. Cróquer, A., C. Bastidas, and D. Lipscomb. 2006. Folliculinid ciliates: a new threat to Caribbean corals? Dis. Aquat. Org. 69:75-78.
8. Dolan, J. R., and M. T. Pérez. 2000. Costs, benefits and characteristics of mixotrophy in marine oligotrichs. Freshw. Biol. 45:227-238.
9. Dunn, S. R., J. C. Bythell, M. D. A. Le Tissier, W. J. Burnett, and J. C. Thomason. 2002. Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the sea anemone Aiptasia sp. J. Exp. Mar. Biol. Ecol. 272:29-53.
10. Enriquez, S., E. R. Méndez, and R. Iglesias-Prieto. 2005. Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50:1025-1032.
11. Fenchel, T. 1987. Ecology of protozoa. Science Tech Publishers, Madison, WI.
12. Fenchel, T., and R. N. Glud. 1998. Veil architecture in a sulphide-oxidizing bacterium enhances countercurrent flux. Nature 394:367-369.
13. Franklin, D. J., O. Hoegh-Gulberg, R. J. Jones, and J. A. Berges. 2004. Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar. Ecol. Prog. Ser. 272:117-130.
14. Freudenthal, H. D. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J. Protozool. 9:45-52.
15. Frias-Lopez, J., A. Zerkle, G. T. Bonheyo, and B. W. Fouke. 2002. Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl. Environ. Microbiol. 68:2214-2228.
16. Glud, R. N., J. K. Gundersen, N. P. Revsbech, and B. B. Jørgensen. 1994. Effects on the benthic diffusive boundary layer imposed by microelectrodes. Limnol. Oceanogr. 39:462-467.
17. Glud, R. N., and T. Fenchel. 1999. The importance of ciliates for interstitial solute transport in benthic communities. Mar. Ecol. Prog. Ser. 186:87-93.
18. Goff, L. J., and J. R. Stein. 1981. Digestion in the peritrich ciliate Ophrydium versatile. Protoplasma 107:235-254.
19. Harvell, C. D., K. Kim, J. M. Burkholder, R. R. Colwell, P. R. Epstein, D. J. Grimes, E. E. Hofmann, E. K. Lipp, A. D. M. E. Osterhaus, R. M. Overstreet, J. W. Porter, G. W. Smith, and G. R. Vasta. 1999. Emerging marine disease-climate links and anthropogenic factors. Science 285:1505-1510.
20. Harvell, C. D., C. E. Mitchell, J. R. Ward, S. Altizer, A. P. Dobson, R. S. Ostfeld, and M. D. Samuel. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296:2158-2162.
21. Hasson, K. W., J. Hasson, H. Aubert, R. M. Redman, and D. V. Lightner. 1997. A new RNA-friendly fixative for the preservation of penaeid shrimp samples for virological detection using cDNA genomic probes. J. Virol. Methods 66:227-236.
22. Hill, R., U. Schreiber, R. Gademann, A. W. D. Larkum, M. Kühl, and P. J. Ralph. 2004. Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching conditions in three species of coral. Mar. Biol. 144:633-640.
23. Hill, R., C. Frankart, and P. J. Ralph. 2005. Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. J. Exp. Mar. Biol. Ecol. 322:83-92.
24. Iglesias-Prieto, R., V. H. Beltran, T. C. Lajeunesse, H. Reyes-Bonilla, and P. E. Thome. 2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc. R. Soc. Lond. B 271: 1757-1763.
25. 2, pH and light. Mar. Ecol. Prog. Ser. 117:159-172.
26. Kühl, M., R. N. Glud, H. Ploug, and N. B. Ramsing. 1996. Microenvironmental control of photosynthesis and photosynthesis-coupled respiration in an epilithic cyanobacterial biofilm. J. Phycol. 32:799-812.
27. 2 microsensors. Mar. Ecol. Prog. Ser. 223:1-14.
28. Lafferty, K. D., J. Porter, and S. E. Ford. 2004. Are diseases increasing in the oceans? Annu. Rev. Ecol. Evol. Syst. 35:31-54.
29. Lobban, C. S., M. Schefter, A. G. B. Simpson, X. Pochon, J. Pawlowski, and W. Foissner. 2002. Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Mar. Biol. 141:207-208.
30. Lobban, C. S., L. Modeo, F. Verni, and G. Rosati. 2005. Euplotes uncinatus (Ciliophora, Hypotrichia), a new species with zooxanthellae. Mar. Biol. 147: 1055-1061.
31. McClanahan, T. R., and N. A. Muthiga. 1998. An ecological shift in a remote coral atoll of Belize over 25 years. Environ. Conserv. 25:122-130.
32. Nishiyama, Y., H. Yamamoto, S. I. Allakhverdiev, M. Inaba, A. Yokota, and N. Murata. 2001. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J. 20:5587-5594.
33. Pantos, O., R. P. Cooney, M. D. A. Le Tissier, M. R. Barer, A. G. O'Donnell, and J. C. Bythell. 2003. The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ. Microbiol. 5: 370-382.
34. Patterson, K. L., J. W. Porter, K. B. Ritchie, S. W. Polson, E. Mueller, E. C. Peters, D. L. Santavy, and G. W. Smith. 2002. The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc. Natl. Acad. Sci. USA 99:8725-8730.
35. Platt, T., C. L. Gallegos, and W. G. Harrison. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38:687-701.
36. Ralph, P. J., R. Gademann, A. W. D. Larkum, and M. Kühl. 2002. Spatial heterogeneity in active chlorophyll fluorescence and PSII activity of coral tissues. Mar. Biol. 141:639-646.
37. Ralph, P. J., U. Schreiber, R. Gademann, M. Kühl, and A. W. D. Larkum. 2005. Coral photobiology studied with a new imaging pulse amplitude modulated fluorometer. J. Phycol. 41:335-342.
38. Rasmussen, L. 1974. Food vacuole membrane in nutrient uptake by Tetrahymena. Nature 250:157-158.
39. Revsbech, N. P. 1989. An oxygen microelectrode with a guard cathode. Limnol. Oceanogr. 34:474-478.
40. Revsbech, N. P., and B. B. Jørgensen. 1983. Photosynthesis of benthic microflora measured with high spatial resolution by the oxygen microprofile method: capabilities and limitations of the method. Limnol. Oceanogr. 28: 749-756.
41. Richardson, L. L. 1997. Black band disease, p. 325-349. In E. Rosenberg and Y. Loya (ed.), Coral health and disease. Springer-Verlag, New York, NY.
42. Rohwer, F., M. Breitbart, J. Jara, F. Azam, and N. Knowlton. 2001. Diversity of bacteria associated with the Caribbean coral Montastraea franski. Coral Reefs 20:85-91.
43. Rohwer, F., V. Seguritan, F. Azam, and N. Knowlton. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1-10.
44. Rosenberg, E., and Y. Ben-Haim. 2002. Microbial diseases of corals and global warming. Environ. Microbiol. 4:318-326.
45. Schreiber, U. 2004. Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview, p. 279-319. In G. C. Papageorgiou and Govindjee (ed.), Chlorophyll fluorescence: a signature of photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands.
46. Shick, J. M., C. Ferrier-Pages, R. Grover, and D. Allemand. 2005. Effects of starvation, ammonium concentration, and photosynthesis on the UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata. Mar. Ecol. Prog. Ser. 295:135-156.
47. Sommaruga, R., K. Whitehead, J. M. Shick, and C. S. Lobban. 2006. Mycosporine-like amino acids in the zooxanthella-ciliate symbiosis Maristentor dinoferus. Protist 157:185-191.
48. Stoecker, D. K., M. W. Silver, A. E. Michaels, and L. H. Davis. 1988. Obligate mixotrophy in Laboea strobila, a ciliate which retains chloroplasts. Mar. Biol. 99:415-423.
49. Stoecker, D. K., M. W. Silver, A. E. Michaels, and L. H. Davis. 1989. Enslavement of algal chloroplasts by four Strombidium spp. Mar. Microb. Food Webs 3:79-100.
50. Stoecker, D. K., and M. W. Silver. 1990. Replacement and aging of chloroplasts in Strombidium capitatum (Ciliophora: Oligotrichida). Mar. Biol. 107: 491-502.
51. Stoecker, D. K. 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J. Protistol. 34:281-290.
52. Thar, R., and M. Kühl. 2002. Conspicuous veils formed by vibrioid bacteria on sulfidic marine sediment. Appl. Environ. Microbiol. 68:6310-6320.
53. Ulstrup, K. E., P. J. Ralph, A. W. D. Larkum, and M. Kühl. 2006. Intracolonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar. Biol. 149:1325-1335.
54. Williams, E. H., and L. Bunkley-Williams. 1990. The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Res. Bull. 335: 1-71.
55. Willis, B. L., C. A. Page, and E. A. Dinsdale. 2004. Coral disease in the Great Barrier Reef, p. 69-104. In E. Rosenberg and Y. Loya (ed.), Coral health and disease. Springer-Verlag, New York, NY.
56. Winkler, R., A. Antonius, and D. A. Renegar. 2004. The skeleton eroding band disease on coral reefs of Aqaba, Red Sea. Mar. Ecol. 25:129-144.