Thermal and sedimentation stress are unlikely causes of brown spot syndrome in the Coral Reef sponge, Ianthella basta

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Luter, Heidi M ^a,b,c   Whalan, Steve ^d   Webster, Nicole S ^a  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c CHARLES DARWIN UNIVERSITY   (Australia)

^d SOUTHERN CROSS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

SEA WATER;

ALPHAPROTEOBACTERIA; ARTICLE; BROWN SPOT; CAUSAL ATTRIBUTION; COMMUNITY STRUCTURE; CONTROLLED STUDY; CORAL REEF; ENVIRONMENTAL STRESS; GAMMAPROTEOBACTERIA; HIGH TEMPERATURE; LANTHELLA BASTA; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; SEDIMENTATION; SPONGE (PORIFERA); SYMBIONT; TEMPERATURE SENSITIVITY; THAUMARCHAEOTA; TIME OF DEATH; TISSUE NECROSIS;

ANIMALS; ANTHOZOA; GEOLOGIC SEDIMENTS; TEMPERATURE;

EID: 84862665620     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039779     Document Type: Article

References (73)

1. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al. (2011) Assessing the complex sponge microbiota-core, variable and species-specific bacterial communities in marine sponges. ISME Journal doi:10.1038/ismej.2011.116.
2. Taylor MW, Radax R, Steger D, Wagner M, (2007) Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews 71: 295-347.
3. Webster NS, Taylor MW, (2012) Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology 14: 335-346.
4. Bayer K, Schmitt S, Hentschel U, (2008) Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environmental Microbiology 10: 2942-2955.
5. Mohamed NM, Rao V, Hamann MT, Kelly M, Hill RT, (2008) Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Applied and Environmental Microbiology 74: 1209-1222.
6. Off S, Alawi M, Spieck E, (2010) Enrichment and physiological characterization of a novel Nitrospira-like bacterium obtained from a marine sponge. Applied and Environmental Microbiology 76: 4640-4646.
7. Schläppy M, Schöttner SI, Lavik G, Kuypers MMM, de Beer D, et al. (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Marine Biology 157: 593-602.
8. Southwell MW, Popp BN, Martens CS, (2008) Nitrification controls on fluxes and isotopic composition of nitrate from Florida Keys sponges. Marine Chemistry 108: 96-108.
9. Southwell MW, Weisz J, Martens CS, Lindquist N, (2008) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnology and Oceanography 53: 986-996.
10. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, et al. (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environmental Microbiology 10: 1087-1094.
11. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, et al. (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environmental Microbiology 11: 2228-2249.
12. Mohamed NM, Saito K, Tal Y, Hill RT, (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME Journal 4: 38-48.
13. Webster NS, Xavier JR, Freckelton M, Motti CA, Cobb R, (2008) Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environmental Microbiology 10: 3366-3376.
14. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U, (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiology Ecology 38: 105-113.
15. Thoms C, Horn M, Wagner M, Hentschel U, Proksch P, (2003) Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Marine Biology 142: 685-692.
16. Lemoine N, Buell N, Hill A, Hill M, (2007) Assessing the utility of sponge microbial symbiont communities as models to study global climate change: a case study with Halichondria bowerbanki. In: Custódio MR, G L-H, Hajdu E, Muricy G, editors. pp. 419-425 editors. 7th International Sponge Symposium. Rio de Janeiro.
17. López-Legentil S, Song B, McMurray SE, Pawlik JR, (2008) Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Molecular Ecology 17: 1840-1849.
18. Webster NS, Cobb RE, Negri AP, (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME Journal 2: 830-842.
19. Selvin J, Shangmugha Priya S, Seghal Kiran G, Thangavelu T, Sapna Bai N, (2009) Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiological Research 164: 352-363.
20. Webster NS, Webb RI, Ridd MJ, Hill RT, Negri AP, (2001) The effects of copper on the microbial community of a coral reef sponge. Environmental Microbiology 3: 19-31.
21. Haapkylä J, Unsworth RKF, Flavell M, Bourne DG, Schaffelke B, et al. (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS ONE 6: e16893.
22. Harvell CD, Altizer S, Cattadori IM, Harrington L, Weil E, (2009) Climate change and wildlife diseases: When does the host matter the most? Ecology 90: 912-920.
23. Webster NS, (2007) Sponge disease: a global threat? Environmental Microbiology 9: 1363-1375.
24. Galstoff PS, (1942) Wasting disease causing mortality of sponges in the West Indies and Gulf of Mexico. Proceedings VIII American Science Congress. Wahington, D. C: 411-421.
25. Gaino E, Pronzato R, Corriero G, Buffa P, (1992) Mortality of commercial sponges - incidence in 2 Mediterranean areas. Bollettino Di Zoologia 59: 79-85.
26. Vacelet J, (1994) Control of the severe sponge epidemic. Near East and Europe: Algeria, Cyprus, Egypt, Lebanon, Malta, Morocco, Syria, Tunisia, Turkey, Yugoslavia. Technical Report - the struggle against the epidemic which is decimating Mediterranean sponges FI: TCP/RAB/8853. Rome, Italy. 1-39 p.
27. Cerrano C, Bavestrello G, Bianchi CN, Cattaneovietti R, Bava S, et al. (2000) A catstrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-Western Mediterranean), summer 1999. Ecology Letters 3: 284-293.
28. Vicente VP, (1989) Regional commercial sponge extinction in the West Indies: are recent climatic changes responsible? Marine Ecology-Progress Series 10: 179-191.
29. Cebrian E, Uriz MJ, Garrabou J, Ballesteros E, (2011) Sponge mass mortalities in a warming Mediterranean Sea: Are cyanobacteria-harboring species worse off? PLoS ONE 6: e20211.
30. Gerrodette T, Flechsig AO, (1979) Sediment-induced reduction in the pumping rate of the tropical sponge Verongia lacunosa. Marine Biology 55: 103-110.
31. Reiswig HM, (1971) In situ pumping activities of tropical demospongiae. Marine Biology 9: 38-50.
32. Tompkins-MacDonald G, Leys S, (2008) Glass sponges arrest pumping in response to sediment: implications for the physiology of the Hexactinellid conduction system. Marine Biology 154: 973-984.
33. Bannister RJ, Battershill CN, de Nys R, (2012) Suspended sediment grain size and mineralogy across the continental shelf of the Great Barrier Reef: Impacts on the physiology of a coral reef sponge. Continental Shelf Research 32: 86-95.
34. Roberts DE, Davis AR, Cummins SP, (2006) Experimental manipulation of shade, silt, nutrients and salinity on the temperate reef sponge Cymbastela concentrica. Marine Ecology Progress Series 307: 143-154.
35. Whalan S, Battershill C, de Nys R, (2007) Variability in reproductive output across a water quality gradient for a tropical marine sponge. Marine Biology 153: 163-169.
36. Maldonado M, Giraud K, Carmona C, (2008) Effects of sediment on the survival of asexually produced sponge recruits. Marine Biology 154: 631-641.
37. Abdul Wahab MA, de Nys R, Whalan S, (2012) Closing the lifecycle for the sustainable aquaculture of the bath sponge Coscinoderma matthewsi. Aquaculture 324-325: 281-285.
38. Solomon S, Qin D, Manning M, Chen Z, Marquis M, et al. (2007) Climate Change 2007: The Physical Science Basis. Contribution of working group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge.
39. Hoegh-Gulberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
40. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL, (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333: 418-422.
41. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology 5: 1220-1227.
42. Dalton SJ, Godwin S, Smith SDA, Pereg L, (2010) Australian subtropical white syndrome: a transmissible, temperature-dependent coral disease. Marine and Freshwater Research 61: 342-350.
43. Sato Y, Bourne DG, Willis BL, (2011) Effects of temperature and light on the progression of black band disease on the reef coral, Montipora hispida. Coral Reefs 30: 753-761.
44. Weber M, Lott C, Fabricius KE, (2006) Sedimentation stress in a scleractinian coral exposed to terrestrial and marine sediments with contrasting physical, organic and geochemical properties. Journal of Experimental Marine Biology and Ecology 336: 18-32.
45. Littman R, Willis BL, Bourne DG, (2011) Metagenomic analysis of the coral holobiont during a natural bleaching even on the Great Barrier Reef. Environmental Microbiology Reports 3: 651-660.
46. Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, et al. (2009) Metagenomic analysis of stressed coral holobionts. Environmental Microbiology 11: 2148-2163.
47. Przeslawski R, Ahyong S, Byrne M, Worheide G, Hutchings P, (2008) Beyond coral and fish: the effects of climate change on non-coral benthic invertebrates of tropical reefs. Global Climate Change 14: 2773-2795.
48. Luter HM, Whalan S, Webster NS, (2010) Prevalence of tissue necrosis and brown spot lesions in a common marine sponge. Marine and Freshwater Research 61: 484-489.
49. Luter HM, Whalan S, Webster NS, (2010) Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Applied and Environmental Microbiology 76: 5736-5744.
50. Louden D, Whalan S, Evans-Illidge E, Wolff C, de Nys R, (2007) An assessment of the aquaculture potential of the tropical sponges Rhopaloeides odorabile and Coscinoderma sp. Aquaculture 270: 57-67.
51. Reiswig HM, (1971) Particle feeding in natural populations of 3 marine Demosponges. Biological Bulletin 141: 568-591.
52. Berkelmans R, De' ath G, Kininmonth S, Skirving WJ, (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23: 74-83.
53. Flores F, Hoogenboom MO, Smith LD, Cooper TF, Abrego D, et al. (2012) Chronic exposure of corals to fine sediments: lethal and sub-lethal impacts. PLoS ONE. DOI:10.1371/journal.pone.0037795.
54. Ferris MJ, Muyzer G, Ward DM, (1996) Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Applied and Environmental Microbiology 62: 340-346.
55. Muyzer G, de Waal EC, Uitterlinden AG, (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59: 695-700.
56. Marchesi JR, Sata T, Weightman AJ, Martine TA, Fry JC, et al. (1998) Design and Evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Applied and Environmental Microbiology 64: 795-799.
57. Lane DJ, (1991) 16S rRNA sequencing. In: Stackerbrandt E, Goodfellow M, editors. pp. 115-148 editors. Nucleic acid techniques in bacterial systematics. New York: John Wiley and Sons, Inc.
58. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
59. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, et al. (2006) Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Applied and Environmental Microbiology 172: 5069-5072.
60. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Research 32: 1363-1371.
61. Felsenstein J, (1993) PHYLIP (Phylogenetic Inference Package) version 3.5c. Department of Genetics, University of Washington, Seattle.
62. Webster NS, Botté ES, Soo RM, Whalan S, (2011) The larval sponge holobiont exhibits high thermal tolerance. Environmental Microbiology Reports 3: 756-762.
63. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW, (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Applied and Environmental Microbiology 68: 2214-2228.
64. Pantos O, Bythell JC, (2006) Bacterial community structure associated with white band disease in the elkhorn coral Acropora palmata determined using culture independent 16S rRNA techniques. Diseases of Aquatic Organisms 69: 79-88.
65. Kelman D, Kashman Y, Rosenberg E, Ilan M, Ifrach I, et al. (2001) Antimicrobial activity of the reef sponge Amphimedon viridis from the Red Sea: evidence for selective toxicity. Aquatic Microbial Ecology 24: 9-16.
66. Freckelton ML, Luter HM, Andreakis N, Webster NS, Motti CA, (2011) Qualitative variation in colour morphotypes of Ianthella basta (Porifera: Verongida). Hydrobiologia. DOI: 10.1007/s10750-011-0818-x.
67. Pettit GR, Butler MS, Williams MD, Filiatrault MJ, Pettit RK, (1996) Isolation and structure of hemibastadinols 1-3 from the Papua New Guinea marine sponge Ianthella basta. Journal of Natural Products 59: 927-934.
68. Philipp E, Fabricius K, (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. Journal of Experimental Marine Biology and Ecology 287: 57-78.
69. Bergquist PR, Kelly-Borges M, (1995) Systematics and biogeography of the genus Ianthella (Demospongiae: Verongida: Ianthellidae) in the south-west Pacific. Records of the Museums and Art Galleries of the Northern Territory 12: 151-176.
70. Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD, (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environmental Microbiology 6: 121-130.
71. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S, Steinberg PD, (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environmental Microbiology 7: 419-433.
72. Webster NS, Negri AP, Munro M, Battershill CN, (2004) Diverse microbial communities inhabit Antarctic sponges. Environmental Microbiology 6: 288-300.
73. Webster NS, Taylor MW, Behnam F, Lücker S, Rattel T, et al. (2010) Deep sequencing reveals exceptional diver- sity and modes of transmission for bacterial sponge symbionts. Environmental Microbiology 12: 2070-2082.