Sponge-Microbe Associations Survive High Nutrients and Temperatures

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Simister, Rachel ^a   Taylor, Michael W ^a   Tsai, Peter ^b   Webster, Nicole ^c  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; RNA 16S;

ACIDIFICATION; ANIMAL TISSUE; ARTICLE; BENTHOS; COASTAL WATERS; COMMUNITY DYNAMICS; CORAL REEF; DENATURING GRADIENT GEL ELECTROPHORESIS; ENVIRONMENTAL STRESS; EUTROPHICATION; FILTRATION; GENE LIBRARY; GENE SEQUENCE; HEALTH STATUS; HOST; MARINE SPECIES; MICROBIAL COMMUNITY; MICROORGANISM; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT; PELAGIC ZONE; RHOPALOEIDES ODORABILE; SEA; SEA SURFACE TEMPERATURE; SEQUENCE HOMOLOGY; SPONGE (PORIFERA); SURVIVAL; SYMBIONT; SYMBIOSIS; TAXONOMY; THAUMARCHAEOTA; WATER QUALITY;

ANIMALS; DENATURING GRADIENT GEL ELECTROPHORESIS; PORIFERA; RNA, RIBOSOMAL, 16S; SYMBIOSIS; TEMPERATURE;

ANTHOZOA; ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; OTUS; RHOPALOEIDES ODORABILE;

EID: 84871420177     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052220     Document Type: Article

References (121)

1. Brodie J, Devlin M, Haynes D, Waterhouse J, (2011) Assessment of the eutrophication status of the Great Barrier Reef lagoon (Australia). Biogeochemistry 106: 281-302.
2. Brodie JE, Kroon FJ, Schaffelke B, Wolanski EC, Lewis SE, et al. (2012) Terrestrial pollutant runoff to the Great Barrier Reef: An update of issues, priorities and management responses. Mar Pollut Bull 65: 81-100.
3. Brodie J, Waterhouse J, (2012) A critical review of environmental management of the 'not so Great' Barrier Reef. Estuar Coast Shelf S 104-105: 1-22.
4. Schaffelke B, Carleton J, Skuza M, Zagorskis I, Furnas MJ, (2012) Water quality in the inshore Great Barrier Reef lagoon: Implications for long-term monitoring and management. Mar Pollut Bull 65: 249-260.
5. De'ath G, Fabricius K, (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20: 840-850.
6. Devlin MJ, Brodie J, (2005) Terrestrial discharge into the Great Barrier Reef Lagoon: nutrient behavior in coastal waters. Mar Pollut Bull 51: 9-22.
7. Webster AJ, Bartley R, Armour JD, Brodie JE, Thorburn PJ, (2012) Reducing dissolved inorganic nitrogen in surface runoff water from sugarcane production systems. Mar Pollut Bull 65: 128-135.
8. Kroon FJ, (2012) Towards ecologically relevant targets for river pollutant loads to the Great Barrier Reef. Mar Pollut Bull 65: 261-266.
9. Brodie J, Furnas MJ (1996) Cyclones, river flood plumes and natural water quality extremes in the Great Barrier Reef In; HM, Hunter, AG.Eyles and GE.Rayment; Downstream Effects of Land Use. Queensland Department of Natural Resources. 367-374.
10. Brodie J, Schroeder T, Rohde K, Faithful J, Masters B, et al. (2010) Dispersal of suspended sediments and nutrients in the Great Barrier Reef lagoon during river-discharge events: conclusions from satellite remote sensing and concurrent flood-plume sampling. Mar Freshw Res 61: 651-664.
11. Brodie J, Mitchell A, (2005) Nutrients in Australian tropical rivers: changes with agricultural development and implications for receiving environments. Mar Freshw Res 56: 279-302.
12. Devlin MJ, Waterhouse J, Taylor J, Brodie JE (2001) Flood plumes in the Great Barrier Reef: spatial and temporal patterns in composition and distribution. GBRMPA Research Publication No 68.
13. Crow JM (2011) Queensland floods hit Great Barrier Reef. Nature News. Nature: doi:10.1038/news.2011.21.
14. Emanuel K, (2005) Increasing destructiveness of tropical cyclones over the past 30 years. Nature 436: 686-688.
15. Klotzbach PJ (2006) Trends in global tropical cyclone activity over the past twenty years (1986-2005). Geophys Res Lett 33.
16. Bell JJ, (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79: 341-353.
17. Taylor MW, Radax R, Steger D, Wagner M, (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
18. Hentschel U, Piel J, Degnan SM, Taylor MW, (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10: 641-654.
19. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, et al. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
20. Schmitt S, Hentschel U, Taylor M, (2012) Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia 687: 341-351.
21. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, et al. (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431-4440.
22. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW, (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14: 517-524.
23. Taylor MW, Tsai P, Simister R, Deines P, Botte E, et al. (2012) "Sponge-specific" bacteria are widespread (but rare) in diverse marine environments. ISME J. doi: 10.1038/ismej.2012.111.
24. Wilkinson CR, Fay P, (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279: 527-529.
25. Weisz J, Hentschel U, Lindquist N, Martens C, (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol 152: 475-483.
26. Mohamed NM, Colman AS, Tal Y, Hill RT, (2008) Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ Microbiol 10: 2910-2921.
27. Mohamed NM, Saito K, Tal Y, Hill RT, (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4: 38-48.
28. Preston CM, Wu KY, Molinski TF, Delong EF, (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci U S A 93: 6241-6246.
29. Radax R, Hoffmann F, Rapp HT, Leininger S, Schleper C, (2012) Ammonia-oxidizing archaea as main drivers of nitrification in cold-water sponges. Environ Microbiol 14: 909-923.
30. Bayer K, Schmitt S, Hentschel U, (2008) Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environ Microbiol 10: 2942-2955.
31. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, et al. (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11: 2228-2243.
32. Diaz MC, Akob D, Cary CS, (2004) Denaturing gradient gel electrophoresis of nitrifying microbes associated with tropical sponges. Boll Mus Ist Biol Univ Genova 68: 279-289.
33. Off S, Alawi M, Spieck E, (2010) Enrichment and physiological characterization of a novel nitrospira-like bacterium obtained from a marine sponge. Appl Environ Microbiol 76: 4640-4646.
34. Schläppy M-L, Schöttner S, Lavik G, Kuypers M, de Beer D, et al. (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157: 593-602.
35. Fiore CL, Jarett JK, Olson ND, Lesser MP, (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 18: 455-463.
36. Bruno JF, Petes LE, Drew Harvell C, Hettinger A, (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6: 1056-1061.
37. Kim K, Harvell CD (2002) Aspergillosis of sea fan corals: Disease dynamics in the Florida Keys. The Everglades, Florida Bay, and Coral Reefs of the Florida Keys: An Ecosystem Sourcebook: 813-824.
38. Fabricius KE, (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50: 125-146.
39. Koop K, Booth D, Broadbent A, Brodie J, Bucher D, et al. (2001) ENCORE: The Effect of Nutrient Enrichment on Coral Reefs. Synthesis of Results and Conclusions. Mar Pollut Bull 42: 91-120.
40. Kaczmarsky L, Richardson L, (2011) Do elevated nutrients and organic carbon on Philippine reefs increase the prevalence of coral disease? Coral Reefs 30: 253-257.
41. Looney EE, Sutherland KP, Lipp EK, (2010) Effects of temperature, nutrients, organic matter and coral mucus on the survival of the coral pathogen, Serratia marcescens PDL100. Environ Microbiol 12: 2479-2485.
42. Voss J, Richardson L, (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25: 569-576.
43. Garren M, Azam F, (2012) Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment. ISME J 6: 1159-1165.
44. Garren M, Raymundo L, Guest J, Harvell CD, Azam F, (2009) Resilience of coral-associated bacterial communities exposed to fish farm effluent. PLoS One 4: e7319.
45. Kline DI, Kuntz NM, Breitbart M, Knowlton N, Rohwer F, (2006) Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314: 119-125.
46. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, et al. (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9: 835-845.
47. Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, et al. (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148-2163.
48. Nogales B, Lanfranconi MP, Piña-Villalonga JM, Bosch R, (2011) Anthropogenic perturbations in marine microbial communities. FEMS Microbiol Rev 35: 275-298.
49. Crump BC, Peranteau C, Beckingham B, Cornwell JC, (2007) Respiratory succession and community succession of bacterioplankton in seasonally anoxic estuarine waters. Appl Environ Microbiol 73: 6802-6810.
50. Morris RM, Vergin KL, Cho JC, Rappé MS, Carlson CA, et al. (2005) Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnol Oceanogr 50: 1687-1696.
51. Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, et al. (2009) Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J 3: 283-295.
52. Shi Y, McCarren J, DeLong EF, (2012) Transcriptional responses of surface water marine microbial assemblages to deep-sea water amendment. Environ Microbiol 14: 191-206.
53. Schäfer H, Bernard L, Courties C, Lebaron P, Servais P, et al. (2001) Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations. FEMS Microbiol Ecol 34: 243-253.
54. Teira E, Martínez-García S, Calvo-Díaz A, Morán XAG, (2010) Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the Atlantic Ocean. Aquat Microb Ecol 60: 299-313.
55. Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, et al. (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30: 19-36.
56. Sipura J, Haukka K, Helminen H, Lagus A, Suomela J, et al. (2005) Effect of nutrient enrichment on bacterioplankton biomass and community composition in mesocosms in the Archipelago Sea, northern Baltic. J Plankton Res 27: 1261-1272.
57. Øvreås L, Bourne D, Sandaa R-A, Casamayor EO, Benlloch S, et al. (2003) Response of bacterial and viral communities to nutrient manipulations in seawater mesocosms. Aquat Microb Ecol 31: 109-121.
58. Witt V, Wild C, Uthicke S, (2012) Interactive climate change and runoff effects alter O2 fluxes and bacterial community composition of coastal biofilms from the Great Barrier Reef. Aquat Microb Ecol 66: 117-131.
59. Negri AP, Hoogenboom MO, (2011) Water Contamination Reduces the Tolerance of Coral Larvae to Thermal Stress. PLoS One 6: e19703.
60. Uthicke S, Vogel N, Doyle J, Schmidt C, Humphrey C, (2012) Interactive effects of climate change and eutrophication on the dinoflagellate-bearing benthic foraminifer Marginopora vertebralis. Coral Reefs 31: 401-414.
61. Wiedenmann J, D'Angelo C, Smith EG, Hunt AN, Legiret F-E, et al. (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nature Clim Change doi:10.1038/nclimate1661.
62. 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, Lôbo-Hajdu G, Hajdu E, Muricy G, editors. Porifera research: biodiversity, innovation and sustainability Série Livros 28, Museu Nacional, Rio de Janeiro.
63. López-Legentil S, Erwin PM, Pawlik JR, Song B, (2010) Effects of sponge bleaching on ammonia-oxidizing archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongia muta. Microb Ecol 60: 561-571.
64. 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. Mol Ecol 17: 1840-1849.
65. 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.
66. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, et al. (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15: 1090-1103.
67. Webster NS, Cobb RE, Negri AP, (2008) Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2: 830-842.
68. Pantile R, Webster N, (2011) Strict thermal threshold identified by quantitative PCR in the sponge Rhopaloeides odorabile. Mar Ecol Prog Ser 431: 97-105.
69. Simister R, Taylor MW, Tsai P, Fan L, Bruxner TJ, et al. (2012) Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge, Rhopaloeides odorabile. Environ Microbiol: doi: 10.1111/1462-2920.12010.
70. 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.
71. Webster NS, Cobb RE, Soo R, Anthony SL, Battershill CN, et al. (2011) Bacterial community dynamics in the marine sponge Rhopaloeides odorabile under in situ and ex situ cultivation. Mar Biotechnol 13: 296-304.
72. Ryle VD, Mueller HR, Gentien P (1981) Automated analysis of nutrients in tropical sea waters. AIMS Oceanography Series Tech Bulletin No3 AIMS OS 81 2: Townsville.
73. Simister RL, Schmitt S, Taylor MW, (2011) Evaluating methods for the preservation and extraction of DNA and RNA for analysis of microbial communities in marine sponges. J Exp Mar Biol Ecol 397: 38-43.
74. Ferris MJ, Muyzer G, Ward DM, (1996) Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62: 340-346.
75. 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. Appl Environ Microbiol 59: 695-700.
76. Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, et al. (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A 103: 12317-12322.
77. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB, (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102: 14683-14688.
78. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications: 315-322.
79. DeLong EF, (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89: 5685-5689.
80. Martinez-Murcia AJ, Acinas SG, Rodriguez-Valera F, (1995) Evaluation of prokaryotic diversity by restrictase digestion of 16S rDNA directly amplified from hypersaline environments. FEMS Microbiol Ecol 17: 247-255.
81. Smit E, Leeflang P, Wernars K, (1997) Detection of shifts in microbial community structure and diversity in soil caused by copper contamination using amplified ribosomal DNA restriction analysis. FEMS Microbiol Ecol 23: 249-261.
82. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
83. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R, (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (16): 2194-2200.
84. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
85. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: A software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
86. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ, (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38 doi:10.1186/1471-2105-1112-1138.
87. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
88. Joachimiak MP, Weisman JL, May BCH, (2006) JColorGrid: Software for the visualization of biological measurements. BMC Bioinformatics 7: 225.
89. Humphrey C, Weber M, Lott C, Cooper T, Fabricius K, (2008) Effects of suspended sediments, dissolved inorganic nutrients and salinity on fertilisation and embryo development in the coral Acropora millepora (Ehrenberg, 1834). Coral Reefs 27: 837-850.
90. Lozupone C, Knight R, (2005) UniFrac: a New Phylogenetic Method for Comparing Microbial Communities. Appl Environ Microbiol 71: 8228-8235.
91. Bannister R (2008) The ecology and feeding biology of the sponge Rhopaloeides odorabile. Thesis for the degree of Doctor of Philosophy in the School of Marine and Tropical Biology, Townsville, JCU.
92. Bannister RJ, Battershill CN, de Nys R, (2010) Demographic variability and long-term change in a coral reef sponge along a cross-shelf gradient of the Great Barrier Reef. Mar Freshw Res 61: 389-396.
93. Bainbridge ZT, Wolanski E, Álvarez-Romero JG, Lewis SE, Brodie JE, (2012) Fine sediment and nutrient dynamics related to particle size and floc formation in a Burdekin River flood plume, Australia. Mar Pollut Bull 65: 236-248.
94. Whalan S, Battershill C, De Nys R, (2007) Variability in reproductive output across a water quality gradient for a tropical marine sponge. Mar Biol 153: 163-169.
95. Allison SD, Martiny JBH, (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105: 11512-11519.
96. Hoegh-Guldberg 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.
97. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL, (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333: 418-422.
98. Gochfeld D, Easson C, Freeman C, Thacker R, Olson J, (2012) Disease and nutrient enrichment as potential stressors on the Caribbean sponge Aplysina cauliformis and its bacterial symbionts. Mar Ecol Prog Ser 456: 101-111.
99. Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A, et al. (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5: 650-664.
100. Webster NS, Botté ES, Soo RM, Whalan S, (2011) The larval sponge holobiont exhibits high thermal tolerance. Environ Microbiol Rep 3: 756-762.
101. Meyer B, Kuever J, (2008) Phylogenetic Diversity and Spatial Distribution of the Microbial Community Associated with the Caribbean Deep-water Sponge Polymastia cf. corticata by 16S rRNA, aprA, and amoA Gene Analysis. Microb Ecol 56: 306-321.
102. Webster NS, Watts JEM, Hill RT, (2001) Detection and phylogenetic analysis of novel crenarchaeote and euryarchaeote 16s ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotechnol 3: 600-608.
103. 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. Environ Microbiol 10: 1087-1094.
104. Leininger S, Urich T, Schloter M, Schwark L, Qi J, et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
105. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, et al. (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9: 1162-1175.
106. Chen Y, Qin B, Teubner K, Dokulil MT, (2003) Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25: 445-453.
107. Hyde KD, Jones EBG, Leaño E, Pointing SB, Poonyth AD, et al. (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7: 1147-1161.
108. Wilkinson CR (1992) Symbiotic interactions between marine sponges and algae. In: W. Reisser (ed.), Algae and symbioses: plants, animals, fungi, viruses, interactions explored. 111-151.
109. Meyer-Reil L-A, Köster M, (2000) Eutrophication of Marine Waters: Effects on Benthic Microbial Communities. Mar Pollut Bull 41: 255-263.
110. Masó M, Garcés E, (2006) Harmful microalgae blooms (HAB); problematic and conditions that induce them. Mar Pollut Bull 53: 620-630.
111. Riegman R, (1995) Nutrient-related selection mechanisms in marine phytoplankton communities and the impact of eutrophication on the planktonic food web. Water Sci Technol 32: 63-75.
112. Caron DA, Lim EL, Sanders RW, Dennett MR, Berninger U-G, (2000) Responses of bacterioplankton and phytoplankton to organic carbon and inorganic nutrient additions in contrasting oceanic ecosystems. Aquat Microb Ecol 22: 175-184.
113. Roberts DE, Davis AR, Cummins SP, (2006) Experimental manipulation of shade, silt, nutrients and salinity on the temperate reef sponge Cymbastela concentrica. Mar Ecol Prog Ser 307: 143-154.
114. IPCC (2007) Climate Change 2007: The physical basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change: Geneva Cambridge, UK: Cambridge University Press.
115. Massaro AJ, Weisz JB, Hill MS, Webster NS, (2012) Behavioral and morphological changes caused by thermal stress in the Great Barrier Reef sponge Rhopaloeides odorabile. J Exp Mar Biol Ecol 416-417: 55-60.
116. Wooldridge SA, (2009) Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58: 745-751.
117. Ferrier-Pagès C, Gattuso JP, Dallot S, Jaubert J, (2000) Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19: 103-113.
118. Gerrodette T, Flechsig AO, (1979) Sediment-induced reduction in the pumping rate of the tropical sponge Verongia lacunosa. Mar Biol 55: 103-110.
119. 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. Cont Shelf Res 32: 86-95.
120. Cervino JM, Winiarski-Cervino K, Polson SW, Goreau T, Smith GW, (2006) Identification of bacteria associated with a disease affecting the marine sponge Ianthella basta in New Britain, Papua New Guinea. Mar Ecol Prog Ser 324: 139-150.
121. Kroon FJ, Kuhnert PM, Henderson BL, Wilkinson SN, Kinsey-Henderson A, et al. (2012) River loads of suspended solids, nitrogen, phosphorus and herbicides delivered to the Great Barrier Reef lagoon. Mar Pollut Bull 65: 167-181.