Skip to main content
SpringerLink
Log in

Response of Sponge Microbiomes to Environmental Variations

  • Chapter
  • First Online:
Symbiotic Microbiomes of Coral Reefs Sponges and Corals

Abstract

Sponges (phylum Porifera), sessile invertebrates, are the oldest multicellular animals that play an important role in evolutionary study. Thanks to their efficient filter-feeding capabilities, sponges have important ecological and biotechnological functions in nutrient cycles within marine ecosystems. Sponges permanently host remarkable microbial taxa with high diversity and complex structure. The associated microbes have been proved to highly contribute to the host growth and metabolite production, chemical defence, and susceptibility to biotic and abiotic stressors. This chapter will provide a systematic review on the variations of sponge microbiomes in relation to environmental stressors, including physical, chemical, and biological factors; as well as on how the changes in microbial composition cause the host sponge to suffer diseases and the consequent variations of the associated microbial community during a disease outbreak.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, de Voogd NJ, et al. Global diversity of sponges (porifera). PLoS One. 2012;7:e35105.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez B, et al. World porifera database. 2018. Accessed at http://www.marinespecies.org/porifera

  3. Hentschel U, Piel J, Degnan SM, Taylor MW. Genomic insights into the marine sponge microbiome. Nat Rev Microbiol. 2012;10:641–54.

    Article  CAS  PubMed  Google Scholar 

  4. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, et al. Complex nitrogen cycling in the sponge geodia barretti. Environ Microbiol. 2009;11:2228–43.

    Article  CAS  PubMed  Google Scholar 

  5. Mehbub MF, Lei J, Franco CMM, Zhang W. Marine sponge derived natural products between 2001 and 2010: trends and opportunities for discovery of bioactives. Mar Drugs. 2014;12:4539–77.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep. 2013;30:237–323.

    Article  CAS  PubMed  Google Scholar 

  7. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep. 2014;31:160–258.

    Article  CAS  PubMed  Google Scholar 

  8. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep. 2015;32:116–211.

    Article  CAS  PubMed  Google Scholar 

  9. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep. 2016;33:382–431.

    Article  CAS  PubMed  Google Scholar 

  10. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsepd MR. Marine natural products. Nat Prod Rep. 2017;34:235–94.

    Article  CAS  PubMed  Google Scholar 

  11. Thacker RW, Freeman CJ. Sponge–microbe symbioses: recent advances and new directions. Adv Mar Biol. 2012;62:57–111.

    Article  PubMed  Google Scholar 

  12. Webster NS, Taylor MW. Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol. 2012;14:335–46.

    Article  CAS  PubMed  Google Scholar 

  13. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW. Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganism. Environ Microbiol. 2012;14:517–24.

    Article  CAS  PubMed  Google Scholar 

  14. Moitinho-Silva L, Nielsen S, Amir A, Gonzalez A, Ackermann GL, Cerrano C, et al. The sponge microbiome project. GigaScience. 2017;6:1–7.

    Article  CAS  PubMed  Google Scholar 

  15. Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun. 2016;7:11870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gao Z-M, Zhou G-W, Huang H, Wang Y. The cyanobacteria-dominated sponge dactylospongia elegans in the south china sea: Prokaryotic community and metagenomic insights. Front Microbiol. 2017;8:art1387.

    Article  Google Scholar 

  17. López-Legentil S, Erwin PM, Pawlik JR, Song B. 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. 2010;60:561–71.

    Article  CAS  PubMed  Google Scholar 

  18. Slaby BM, Hackl T, Horn H, Bayer K, Hentschel U. Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization. ISME J. 2017;11:2465–78.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Freeman CJ, Thacker RW. Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr. 2011;56:1577–86.

    Article  Google Scholar 

  20. Flatt PM, Gautschi JT, Thacker RW, Musafija-Girt M, Crews P, Gerwick WH. Identification of the cellular site of polychlorinated peptide biosynthesis in the marine sponge Dysidea (lamellodysidea) herbacea and symbiotic cyanobacterium Oscillatoria spongeliae by card-fish analysis. Mar Biol. 2005;147:761–74.

    Article  CAS  Google Scholar 

  21. Marty MJ, Vicente J, Oyler BL, Place A, Hill RT. Sponge symbioses between Xestospongia deweerdtae and Plakortis spp. Are not motivated by shared chemical defense against predators. PLoS One. 2017;12:e0174816.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Webster NS, Xavier JR, Freckelton M, Motti CA, Cobb R. Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ Microbiol. 2008;10:3366–76.

    Article  CAS  PubMed  Google Scholar 

  23. Webster NS, Cobb RE, Negri AP. Temperature thresholds for bacterial symbiosis with a sponge. ISME J. 2008;2:830–42.

    Article  CAS  PubMed  Google Scholar 

  24. Guzman C. Conaco, C Gene expression dynamics accompanying the sponge thermal stress response. PLoS One. 2016;11:e0165368.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Taylor MW, Radax R, Steger D, Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev. 2007;71:295–347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lee YK, Jung HJ, Lee HK. Marine bacteria associated with the korean brown alga, Undaria pinnatifida. J Microbiol. 2006;44:694–8.

    CAS  PubMed  Google Scholar 

  27. Webster NS, Hill RT. The culturable microbial community of the great barrier reef sponge Rhopaloeides odorabile is dominated by an α-proteobacterium. Mar Biol. 2001;138:843–51.

    Article  CAS  Google Scholar 

  28. White JR, Patel J, Ottesen A, Arce G, Blackwelder P, Lopez JV. Pyrosequencing of bacterial symbionts within Axinella corrugata sponges: diversity and seasonal variability. PLoS One. 2012;7:e38204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wichels A, Würtz S, Döpke H, Schütt C, Gerdts G. Bacterial diversity in the breadcrumb sponge Halichondria panicea. FEMS Microb Ecol. 2006;56:102–18.

    Article  CAS  Google Scholar 

  30. Anderson SA, Northcote PT, Page MJ. Spatial and temporal variability of the bacterial community in different chemotypes of the New Zealand marine sponge Mycale hentscheli. FEMS Microbiol Ecol. 2010;72:328–42.

    Article  CAS  PubMed  Google Scholar 

  31. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U. Temporal variation of the microbial community associated with the mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol. 2001;38:105–13.

    Article  CAS  Google Scholar 

  32. Webster NS, Cobb RE, Soo R, Anthony SL, Battershill CN, Whalan S, et al. Bacterial community dynamics in the marine sponge Rhopaloeides odorabile under in situ and ex situ cultivation. Mar Biotechnol. 2011;13:296–304.

    Article  CAS  Google Scholar 

  33. Mohamed NM, Rao V, Hamann MT, Kelly M, Hill RT. Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl Environ Microbiol. 2008;74:4133–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mohamed NM, Enticknap JJ, Lohr JE, McIntosh SM, Hill RT. Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl Environ Microbiol. 2008;74:1209–22.

    Article  CAS  PubMed  Google Scholar 

  35. Cleary DFR, Becking LE, de Voogd NJ, Pires ACC, Polónia ARM, Egas C, et al. Habitat- and host-related variation in sponge bacterial symbiont communities in indonesian waters. FEMS Microbiol Ecol. 2013;85:465–82.

    Article  CAS  PubMed  Google Scholar 

  36. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 2012;6:564–76.

    Article  CAS  PubMed  Google Scholar 

  37. Schmitt S, Hentschel U, Taylor M. Deep sequencing reveals diversity and community structure of complex microbiota in five mediterranean sponges. In: Maldonado M, Turon X, Becerro MA, Uriz MJ, editors. Ancient animals, new challenges: developments in sponge research. Dordrecht: Springer; 2012. p. 341–51.

    Google Scholar 

  38. Burgsdorf I, Erwin PM, López-Legentil S, Cerrano C, Haber M, Frenk S, et al. Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Front Microbiol. 2014;10:1–11.

    Google Scholar 

  39. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, et al. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol. 2002;68:4431–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S, Steinberg PD. Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ Microbiol. 2005;7:419–33.

    Article  CAS  PubMed  Google Scholar 

  41. Cárdenas CA, Bell JJ, Davy SK, Hoggard M, Taylor MW. Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiol Ecol. 2014;88:516–27.

    Article  PubMed  CAS  Google Scholar 

  42. Montalvo NF, Hill RT. Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Enrivon Micorbiol. 2011;77:7207–16.

    Article  CAS  Google Scholar 

  43. Olson JB, Thacker RW, Gochfeld DJ. Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the caribbean sponge aplysina cauliformis. FEMS Microbiol Ecol. 2013;87:268–79.

    Article  PubMed  CAS  Google Scholar 

  44. Erwin PM, Coma R, López-Sendino P, Serrano E, Ribes M. Stable symbionts across the hma-lma dichotomy: low seasonal and interannual variation in sponge-associated bacteria from taxonomically diverse hosts. FEMS Microbiol Ecol. 2015;91:1–11.

    Article  CAS  Google Scholar 

  45. Peek AS, Feldman RA, Lutz R, Vrijenhoek RC. Cospeciation of bacteria and deep sea clams. Proc Natl Acad Sci U S A. 1998;95:9962–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Brusca RC, Brusca GJ. Phylum Porifera: the sponges. In: Sinauer AD, editor. Invertebrates. Cambridge, MA: Sinauer Press; 1990. p. 181–210.

    Google Scholar 

  47. Gallissian MF, Vacelet J. Ultrastructure de quelques stades de l’ovogénèse de spongiaires du genre verongia (dictyoceratida). Ann Sci Nat Zool. 1976;18:381–404.

    Google Scholar 

  48. Vacelet J, Boury-Esnault N, Fiala-Medioni A, Fisher CR. A methanotrophic carnivorous sponge. Nature. 1995;377:296.

    Article  CAS  Google Scholar 

  49. Vogel S. Current-induced flow through living sponges in nature. Proc Natl Acad Sci U S A. 1977;74:2069–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Rappe MS, Vergin K, Giovannoni SJ. Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol Ecol. 2000;33:219–32.

    Article  CAS  PubMed  Google Scholar 

  51. Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, et al. Comparative 16s rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Enrivon Micorbiol. 2000;66:5053–6.

    Article  Google Scholar 

  52. Ravenschlag K, Sahm K, Pernthaler J, Amann R. High bacterial diversity in permanently cold marine sediments. Appl Enrivon Micorbiol. 1999;65:3982–9.

    CAS  Google Scholar 

  53. Turon X, Galera J, Uriz MJ. Clearance rates and aquiferous systems in two sponges with contrasting life-history strategies. J Exp Zool. 1997;278:22–36.

    Article  Google Scholar 

  54. Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, Hentschel U. Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol. 1999;134:461–70.

    Article  Google Scholar 

  55. Wilkinson CR, Garrone R, Vacelet J. Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc R Soc Lond B. 1984;220:519–28.

    Article  Google Scholar 

  56. Turque AS, Cardoso AM, Silveira CB, Vieira RP, Freitas FAD, Albano RM, et al. Bacterial communities of the marine sponges Hymeniacidon heliophila and Polymastia janeirensis and their environment in Rio de janeiro, Brazil. Mar Biol. 2008;155:135–46.

    Article  Google Scholar 

  57. Lafi FF, Garson MJ, Fuerst JA. Culturable bacterial symbionts isolated from two distinct sponge species (Pseudoceratina clavata and Rhabdastrella globostellata) from the Great Barrier Reef display similar phylogenetic diversity. Microb Ecol. 2005;50:213–20.

    Article  CAS  PubMed  Google Scholar 

  58. Sharp KH, Eam B, Faulkner DJ, Haygood MG. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Enrivon Micorbiol. 2007;73:622–9.

    Article  CAS  Google Scholar 

  59. Zhu P, Li Q, Wang G. Unique microbial signatures of the alien hawaiian marine sponge Suberites zeteki. Micorbial Ecol. 2007;55:406–14.

    Article  Google Scholar 

  60. Alex A, Silva V, Vasconcelos V, Antunes A. Evidence of unique and generalist microbes in distantly related sympatric intertidal marine sponges (Porifera: Demospongiae). PLoS One. 2013;8:e80653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Meyer B, Kuever J. 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. Micorbial Ecol. 2008;56:306–21.

    Article  CAS  Google Scholar 

  62. Luter HM, Widder S, Botté ES, Wahab MA, Whalan S, Moitinho-Silva L, et al. Biogeographic variation in the microbiome of the ecologically important sponge, Carteriospongia foliascens. PeerJ. 2015;3:e1435.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Turque AS, Batista D, Silveira CB, Cardoso AM, Vieira RP, Moraes FC, et al. Environmental shaping of sponge associated archaeal communities. PLoS One. 2010;5:e15774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Weigel BL, Erwin PM. Intraspecific variation in microbial symbiont communities of the sun sponge, Hymeniacidon heliophila, from intertidal and subtidal habitats. Appl Enrivon Micorbiol. 2016;82:650–8.

    Article  CAS  Google Scholar 

  65. Reveillaud J, Maignien L, Eren AM, Huber JA, Apprill A, Sogin ML, et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 2014;8:1198–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Noyer C, Casamayor EO, Becerro MA. Environmental heterogeneity and microbial inheritance influence sponge-associated bacterial composition of Spongia lamella. Microb Ecol. 2014;68:611–20.

    Article  PubMed  Google Scholar 

  67. Dethlefsen L, McFall-Ngai MJ, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449:811–8.

    Article  CAS  PubMed  Google Scholar 

  68. Noyer C, Becerro MA. Relationship between genetic, chemical, and bacterial diversity in the atlanto-mediterranean bath sponge Spongia lamella. Hydrobiologia. 2012;687:85–99.

    Article  Google Scholar 

  69. Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser. 2002;243:1–10.

    Article  Google Scholar 

  70. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E. The coral probiotic hypothesis. Environ Microbiol. 2006;8:2068–73.

    Article  CAS  PubMed  Google Scholar 

  71. Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, editors. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge/New York: Cambridge University Press; 2007. p. 1–996.

    Google Scholar 

  72. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, et al. Coral reefs under rapid climate change and ocean acidification. Science. 2007;318:1737–42.

    Article  CAS  PubMed  Google Scholar 

  73. Webster NS, Blackall LL. What do we really know about sponge-microbial symbioses? ISME J. 2009;3:1–3.

    Article  CAS  PubMed  Google Scholar 

  74. López-Legentil S, Song B, Mcmurray SE, Pawlik JR. Bleaching and stress in coral reef ecosystems: Hsp70 expression by the giant barrel sponge Xestospongia muta. Mol Ecol. 2008;17:1840–9.

    Article  PubMed  CAS  Google Scholar 

  75. Lemoine N, Buell N, Hill A, Hill M. 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. Rio de Janeiro: Série Livros/Museu Nacional; 2007. p. 419–25.

    Google Scholar 

  76. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, et al. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol. 2010;12:2070–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M, et al. Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol. 2008;10:1087–94.

    Article  CAS  PubMed  Google Scholar 

  78. Webster NS, Wilson KJ, Blackall LL, Hill RT. Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol. 2001;67:434–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Webster NS, Botté ES, Soo RM, Whalan S. The larval sponge holobiont exhibits high thermal tolerance. Environ Microbiol Rep. 2011;3:756–62.

    Article  PubMed  Google Scholar 

  80. Webster NS, Watts JEM, Hill RT. Detection and phylogenetic analysis of novel crenarchaeote and euryarchaeote 16S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotechnol. 2001;3:600–8.

    Article  CAS  Google Scholar 

  81. Pantile R, Webster N. Strict thermal threshold identified by quantitative PCR in the sponge Rhopaloeides odorabile. Mar Ecol Prog Ser. 2011;431:97–105.

    Article  CAS  Google Scholar 

  82. Simister R, Taylor MW, Tsai P, Fan L, Bruxner TJ, Crowe ML, et al. Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge, Rhopaloeides odorabile. Environ Microbiol. 2012;14:3232–46.

    Article  CAS  PubMed  Google Scholar 

  83. Mao-Jones J, Ritchie KB, Jones LE, Ellner SP. How microbial community composition regulates coral disease development. PLoS Biol. 2010;8:e1000345.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Fan L, Liu M, Simister R, Webster NS, Thomas T. Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J. 2013;7:991–1002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Girvan MS, Campbell CD, Killham K, Prosser JI, Glover LA. Bacterial diversity promotes community stability and functional resilience after perturbation. Environ Microbiol. 2005;7:301–13.

    Article  CAS  PubMed  Google Scholar 

  86. Allison SD, Martiny JB. Colloquium paper: resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A. 2008;105:11512–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Jones SE, Newton RJ, McMahon KD. Evidence for structuring of bacterial community composition by organic carbon source in temperate lakes. Environ Microbiol. 2009;11:2463–72.

    Article  CAS  PubMed  Google Scholar 

  88. Robinson CJ, Bohannan BJ, Young VB. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev. 2010;74:453–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, et al. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010;4:1557–67.

    Article  CAS  PubMed  Google Scholar 

  90. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, et al. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci U S A. 2012;109:E1878–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T. Metaproteogenomic analysis of a community of sponge symbionts. ISME J. 2012;6:1515–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Erwin PM, Pita L, López-Legentil S, Turona X. Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl Environ Microbiol. 2012;78:7358–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Pita L, Erwin PM, Turon X, López-Legentil S. Till death do us part: stable sponge-bacteria associations under thermal and food shortage stresses. PLoS One. 2013;8:e80307.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Pita L, Turon X, López-Legentil S, Erwin PM. Host rules: spatial stability of bacterial communities associated with marine sponges (Ircinia spp.) in the western mediterranean sea. FEMS Microbiol Ecol. 2013;86:268–76.

    Article  CAS  PubMed  Google Scholar 

  95. Erwin PM, López-Legentil S, González-Pech R, Turon X. A specific mix of generalists: bacterial symbionts in mediterranean Ircinia spp. FEMS Microbiol Ecolol. 2012;79:619–37.

    Article  CAS  Google Scholar 

  96. Maldonado M, Sánchez-Tocino L, Navarro C. Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms. Mar Biol. 2010;157:1577–90.

    Article  Google Scholar 

  97. Stabili L, Cardone F, Alifano P, Tredici SM, Piraino S, Corriero G, et al. Epidemic mortality of the sponge Ircinia variabilis (schmidt, 1862) associated to proliferation of a vibrio bacterium. Microb Ecol. 2012;64:802–13.

    Article  PubMed  Google Scholar 

  98. Cebrian E, Uriz MJ, Garrabou J, Ballesteros E. Sponge mass mortalities in a warming mediterranean sea: are cyanobacteria-harboring species worse off? PLoS One. 2011;6:e20211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Schmitt S, Wehrl M, Lindquist N, Weisz JB, Hentschel U. Morphological and molecular analyses of microorganisms in caribbean reef adult sponges and in corresponding reproductive material. In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G, editors. Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro: Série Livros, Museu Nacional; 2007. p. 561–8.

    Google Scholar 

  100. Sacristán-Soriano O, Banaigs B, Becerro MA. Can light intensity cause shifts in natural product and bacterial profiles of the sponge Aplysina aerophoba? Mar Ecol. 2016;37:88–105.

    Article  Google Scholar 

  101. Olson JB, Gao X. Characterizing the bacterial associates of three caribbean sponges along a gradient from shallow to mesophotic depths. FEMS Microbiol Ecol. 2013;85:74–84.

    Article  PubMed  Google Scholar 

  102. Thoms C, Horn M, Wagner M, Hentschel U, Proksch P. Monitoring microbial diversity and natural product profiles of the sponge Aplysina cavernicola following transplantation. Mar Biol. 2003;142:685–92.

    Article  CAS  Google Scholar 

  103. Gerce B, Schwartz T, Voigt M, Rühle S, Kirchen S, Putz A, et al. Morphological, bacterial, and secondary metabolite changes of aplysina aerophoba upon long-term maintenance under artificial conditions. Microb Ecol. 2009;58:865–78.

    Article  PubMed  Google Scholar 

  104. To Isaacs L, Kan J, Nguyen L, Videau P, Anderson MA, Wright TL, et al. Comparison of the bacterial communities of wild and captive sponge clathria prolifera from the chesapeake bay. Mar Biotechnol. 2009;11:758–70.

    Article  CAS  Google Scholar 

  105. Gaino E, Magnino G. Dissociated cells of the calcareous sponge clathrina: a model for investigating cell adhesion and cell motility in vitro. Microsc Res Tech. 1999;15:279–92.

    Article  Google Scholar 

  106. Thoms C, Schupp PJ. Chemical defense strategies in sponges: a review. In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G, editors. Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro: Série Livros/Museu Nacional; 2007. p. 627–37.

    Google Scholar 

  107. Pérez T, Longet D, Schembri T, Rebouillon P, Vacelet J. Effect of 12 years’operation of a sewage treatment plant on trace metal occurrence within a mediterranean commercial sponge (Spongia officinalis, Demospongiae). Marine Poll Bull. 2005;50:301–9.

    Article  CAS  Google Scholar 

  108. Patel B, Balani MC, Patel S. Sponge ‘sentinel’ of heavy metals. Sci Total Environ. 1985;41:143–52.

    Article  CAS  PubMed  Google Scholar 

  109. de Mestre C, Maher W, Roberts D, Broad A, Krikowa F, Davis AR. Sponges as sentinels: patterns of spatial and intra-individual variation in trace metal concentration. Mar Pollut Bull. 2012;64:80–9.

    Article  PubMed  CAS  Google Scholar 

  110. Cebrian E, Uriz MJ, Turon X. Sponges as biomonitors of heavy metals ins patial and temporal surveys in northwestern mediterranean: multispecies comparison. Environ Toxicol Chem. 2007;26:2430–9.

    Article  CAS  PubMed  Google Scholar 

  111. Hansen IV, Weeks JM, Depledge MH. Accumulation of copper, zinc, cadmium and chromium by the marine sponge Halichondria panacea pallas and the implications for biomonitoring. Marine Poll Bull. 1995;31:133–8.

    Article  CAS  Google Scholar 

  112. Webster NS, Webb RI, Ridd MJ, Hill RT, Negri AP. The effects of copper on the microbial community of a coral reef sponge. Environ Microbiol. 2001;3:19–31.

    Article  CAS  PubMed  Google Scholar 

  113. Tian R-M, Wang Y, Bougouffa S, Gao Z-M, Cai L, Zhang W-P, et al. Effect of copper treatment on the composition and function of the bacterial community in the sponge Haliclona cymaeformis. MBio. 2014;5:e01980–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Santos-Gandelman JF, Cruz K, Crane S, Muricy G, Giambiagi-deMarval M, Barkay T, et al. Potential application in mercury bioremediation of a marine sponge-isolated bacilluscereus strain pj1. Curr Microbiol. 2014;69:374–80.

    Article  CAS  PubMed  Google Scholar 

  115. Bauvais C, Zirah S, Piette L, Chaspoul F, Domart-Coulon I, Chapon V, et al. Sponging up metals: bacteria associated with the marine sponge Spongia officinalis. Mar Environ Res. 2015;104:20–30.

    Article  CAS  PubMed  Google Scholar 

  116. Mangano S, Michaud L, Caruso C, Giudice AL. Metal and antibiotic resistance in psychrotrophic bacteria associated with the antarctic sponge Hemigellius pilosus (kirkpatrick, 1907). Polar Biol. 2014;37:227–35.

    Article  Google Scholar 

  117. Wanick RC, de Sousa Barbosa H, Frazão LR, Santelli RE, Arruda MAZ, Coutinho CC. Evaluation of differential protein expression in Haliclona aquarius and sponge-associated microorganisms under cadmium stress. Anal Bioanal Chem. 2013;405:7661–70.

    Article  CAS  PubMed  Google Scholar 

  118. Selvin J, Priya SS, Kiran GS, Thangavelu T, SapnaBai N. Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiol Res. 2009;164:352–63.

    Article  CAS  PubMed  Google Scholar 

  119. Gochfeld DJ, Easson CG, Freeman CJ, Thacker RW, Olson JB. Disease and nutrient enrichment as potential stressors on the caribbean sponge Aplysina cauliformis and its bacterial symbionts. Mar Ecol Prog Ser. 2012;456:101–11.

    Article  CAS  Google Scholar 

  120. Simister R, Taylor MW, Tsai P, Webster N. Sponge-microbe associations survive high nutrients and temperatures. PLoS One. 2012;7:e52220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Luter HM, Gibb K, Webster NS. Eutrophication has no short-term effect on the Cymbastela stipitata holobiont. Font Microbiol. 2014;5:art216.

    Google Scholar 

  122. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature. 2008;454:96–9.

    Article  CAS  PubMed  Google Scholar 

  123. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang. 2011;1:165–9.

    Article  CAS  Google Scholar 

  124. Morrow KM, Bourne DG, Humphrey C, Botté ES, Laffy P, Zaneveld J, et al. Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J. 2015;9:894–908.

    Article  CAS  PubMed  Google Scholar 

  125. Ribes M, Calvo E, Movilla J, Logares R, Coma R, Pelejero C. Restructuring of the sponge microbiome favors tolerance to ocean acidification. Environ Microbiol Rep. 2016;8:536–44.

    Article  CAS  PubMed  Google Scholar 

  126. Tian R-M, Lee OO, Wang Y, Cai L, Bougouffa S, Chiu JMY, et al. Effect of polybrominated diphenyl ether (PBDE) treatment on the composition and function of the bacterial community in the sponge Haliclona cymaeformis. Front Microbiol. 2015;5:1–8.

    Article  CAS  Google Scholar 

  127. Chelossi E, Milaneseb M, Milanoc A, Pronzatob P, Riccardi G. Characterisation and antimicrobial activity of epibiotic bacteria from petrosia ficiformis (Porifera, Demospongiae). J Exp Mar Biol Ecol. 2004;309:21–33.

    Article  CAS  Google Scholar 

  128. Lee OO, Qian P-Y. Chemical control of bacterial epibiosis and larval settlement of Hydroides elegans in the red sponge Mycale adherens. Biofouling. 2003;19:171–80.

    Article  CAS  PubMed  Google Scholar 

  129. Luter HM. The effects of disease and stress on the microbial community of the sponge Ianthella basta. Townsville: School of Marine and Tropical Biology, James Cook University; 2011.

    Google Scholar 

  130. Kaluzhnaya OV, Itskovich VB. Bleaching of baikalian sponge affects the taxonomic composition of symbiotic microorganisms. Russ J Genet. 2015;51:1153–7.

    Article  CAS  Google Scholar 

  131. Denikina NN, Dzyuba EV, Bel’kova NL, Khanaev IV, Feranchuk SI, Makarov MM, et al. The first case of disease of the sponge lubomirskia baicalensis: investigation of its microbiome. Biol Bull. 2016;43:263–70.

    Article  CAS  Google Scholar 

  132. Gao Z-M, Wang Y, Tian R-M, Lee OO, Wong YM, Batang ZB, et al. Pyrosequencing revealed shifts of prokaryotic communities between healthy and disease-like tissues of the red sea sponge crella cyathophora. PeeJ. 2015;3:e890.

    Google Scholar 

  133. Blanquer A, Uriz MJ, Cebrian E, Galand PE. Snapshot of a bacterial microbiome shift during the early symptoms of a massive sponge die-off in the western mediterranean. Front Microbiol. 2016;7:752.

    Article  PubMed  PubMed Central  Google Scholar 

  134. Luter HM, Bannister RJ, Whalan S, Kutti T, Pineda M-C, Webster NS. Microbiome analysis of a disease affecting the deep-sea sponge geodia barretti. FEMS Microbiol Ecol. 2017;93:1–6.

    Article  CAS  Google Scholar 

  135. McClintock JB, Baker BJ, Slattery M, Hamann M, Kopitzke R, Heine J. Chemotactic tube-foot responses of a spongivorous sea star perknaster fuscus to organic extracts from antarctic sponges. J Chem Ecol. 1994;20:859–70.

    Article  CAS  PubMed  Google Scholar 

  136. Wuff JL. Sponge predators may determine differences in sponge fauna between two sets of mangrove cays, Belize Barrier Reef. Atoll Res Bull. 2000;477:251–63.

    Google Scholar 

  137. Santos CP, Coutinho AB, Hajdu E. Spongivory by eucidaris tribuloides from Salvador, Bahia (echinodermata: Echinoidea). J Mar Biol Assoc UK. 2002;82:295–7.

    Article  Google Scholar 

  138. León YL, Bjorndal KA. Selective feeding in the hawksbill turtle, an important predator in coral reef ecosystems. Mar Ecol Prog Ser. 2002;245:249–58.

    Article  Google Scholar 

  139. Knowlton A, Highsmith RC. Nudibranch-sponge feeding dynamics: benefits of symbiont-containing sponge to Archidoris montereyensis (Cooper, 1862) and recovery of nudibranch feeding scars by Halichondria panicea (Pallas, 1766). J Exp Mar Biol Ecol. 2005;327:36–46.

    Article  Google Scholar 

  140. Jones AC, Blum JE, Pawlik JR. Testing for defensive synergy in caribbean sponges: bad taste or glass spicules? J Exp Mar Biol Ecol. 2005;322:67–81.

    Article  Google Scholar 

  141. Bertolino M, Cerrano C, Bavestrello G, Carella M, Pansini M, Calcinai B. Diversity of porifera in the mediterranean coralligenous accretions, with description of a new species. ZooKeys. 2013;336:1–37.

    Article  Google Scholar 

  142. De Caralt S, Bry D, Bontemps N, Turon X, Uriz M-J, Banaigs B. Sources of secondary metabolite variation in dysidea avara (Porifera: Demospongiae): the importance of having good neighbors. Mar Drugs. 2013;11:489–503.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. Arias J, Santos-Acevedo M, Newmark F. Evaluation of the feeding deterrent potential of crude organic extracts from fifteen marine sponges. Bol Invest Mar Cost. 2011;40:293–308.

    Google Scholar 

  144. Esteves AIS, Hardoim CCP, Xavier JR, Gonçalves JMS, Costa R. Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the Northeast Atlantic. FEMS Microbiol Ecol. 2013;85:519–36.

    Article  CAS  PubMed  Google Scholar 

  145. Uriz M-J, Agell G, Blanquer A, Turon X, Casamayor EO. Endosymbiotic calcifying bacteria: a new cue to the origin of calcification in metazoa? Evolution. 2012;66:2993–9.

    Article  PubMed  PubMed Central  Google Scholar 

  146. Garate L, Blanquer A, Uriz M-J. Calcareous spherules produced by intracellular symbiotic bacteria protect the sponge Hemimycale columella from predation better than secondary metabolites. Mar Ecol Prog Ser. 2015;523:81–92.

    Article  Google Scholar 

  147. Gifford S, Dunstan RH, O’Connor W, Roberts T, Toia R. Pearl aquaculture-profitable environmental remediation? Sci Total Environ. 2004;319:27–37.

    Article  CAS  PubMed  Google Scholar 

  148. Osinga R, Tramper J, Wijffels RH. Cultivation of marine sponges. Mar Biotechnol. 1999;1:509–32.

    Article  CAS  Google Scholar 

  149. Reiswig HM. In situ feeding in two shallow water Hexactinellid sponges. In: Rützler K, editor. New perspectives in sponge biology. Washington, DC: Smithsonian institute; 1990. p. 204–510.

    Google Scholar 

  150. Larsen PS, Riisgård HU. The sponge pump. J Theor Biol. 1994;168:3–63.

    Article  Google Scholar 

  151. Riisgård HU, Larsen PS. Filter-feeding in marine macro-invertebrates: pump characteristics, modelling and energy cost. Biol Rev Camb Philos Soc. 1995;70:67–106.

    Article  PubMed  Google Scholar 

  152. Simpson TL. The cell biology of sponges. New York: Springer-Verlag; 1984.

    Book  Google Scholar 

  153. Gifford S, Dunstan RH, O’Connor W, Koller CE, MacFarlane GR. Aquatic zooremediation: deploying animals to remediate contaminated aquatic environments. Trends Biotechnol. 2006;25:60–5.

    Article  PubMed  CAS  Google Scholar 

  154. Vicente VP. Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs. 1990;8:199–202.

    Article  Google Scholar 

  155. Taylor MW, Schupp PJ, Dahllöf I, Kjelleberg S, Steinberg PD. Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol. 2004;6:121–30.

    Article  PubMed  Google Scholar 

  156. Climate change 2001: impacts, adaptation and vulnerability. In: McCarthy, JJ, Canziani OF, Leary NA, Dokken DJ, White KS editors. Contribution of Working Group II to the third assessment report of the Intergovernmental Panel on Climate Change. Cambridge/New York: Cambridge University Press; 2001. p. 1–1033.

    Google Scholar 

  157. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al. Extinction risk from climate change. Nature. 2004;427:145–8.

    Article  CAS  PubMed  Google Scholar 

  158. Bellwood DR, Hughes TP, Folke C, Nystrom M. Confronting the coral reef crisis. Nature. 2004;429:827–33.

    Article  CAS  PubMed  Google Scholar 

  159. Sheppard CRC, Rioja-Nieto R. Sea surface temperature 1871–2099 in 38 cells in the caribbean region. Mar Environ Res. 2005;60:389–96.

    Article  CAS  PubMed  Google Scholar 

  160. McWilliams JP, Côté IM, Gill JA, Sutherland WJ, Watkinson AR. Accelerating impacts of temperature-induced coral bleaching in the caribbean. Ecology. 2005;86:2055–60.

    Article  Google Scholar 

  161. Cerrano C, Magnino G, Sara A, Bavestrello G, Gaino E. Necrosis in a population of petrosia ficiformis (Porifera, demospongiae) in relations with environmental stress. Ital J Zool. 2001;68:131–6.

    Article  Google Scholar 

  162. McMurray SE, Henkel TP, Pawlik JR. Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida keys. Ecology. 2010;91:560–70.

    Article  PubMed  Google Scholar 

  163. Fiore CL, Baker DM, Lesser MP. Nitrogen biogeochemistry in the caribbean sponge, Xestospongia muta: a source or sink of dissolved inorganic nitrogen? PLoS One. 2013;8:e72961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Fiore CL, Jarett JK, Lesser MP. Symbiotic prokaryotic communities from different populations of the giant barrel sponge, Xestospongia muta. Microbiology Open. 2013;2:938–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Lesser MP, Fiore C, Slattery M, Zaneveld J. Climate change stressors destabilize the microbiome of the caribbean barrel sponge, Xestospongia muta. J Exp Mar Biol Ecol. 2016;475:11–8.

    Article  Google Scholar 

  166. Reilly A, Kaferstein F. Food safety hazards and the application of the principles of the hazard analysis and critical control point (HACCP) system for their control in aquaculture production. Aquac Res. 1997;28:735–52.

    Article  Google Scholar 

  167. Reiswig HM. In situ pumping activities of tropical demospongiae. Mar Biol. 1971;9:38–50.

    Article  Google Scholar 

  168. Vacelet J, Donadey C. Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol. 1977;30:301–14.

    Article  Google Scholar 

  169. Gaino E, Pronzato R. Ultrastructural evidence of bacterial damage to Spongia officinalis (Porifera, Demospongiae) fibres. Dis Aquat Org. 1989;6:67–74.

    Article  Google Scholar 

  170. Vacelet J, Vacelet E, Gaino E, Gallissian M-F. Bacterial attack of spongin skeleton during the 1986–1990 mediterranean sponge disease. In: van Soest RWM, van Kempen TMG, Braekman JC, editors. Sponges in time and space. Rotterdam: Balkema AA; 1994. p. 355–62.

    Google Scholar 

  171. Kefalas E, Castritsi-Catharios J, Miliou H. Bacteria associated with the sponge Spongia officinalis as indicators of contamination. Ecol Indic. 2003;2:339–43.

    Article  Google Scholar 

  172. Velho-Pereira S, Furtado I. Retrieval of euryhaline eubacterial and haloarchaeal bionts from nine different benthic sponges: reflection of the bacteriological health of waters of mandapam, India. Indian J Mar Sci. 2014;43:773–83.

    Google Scholar 

  173. Milanese M, Chelossi E, Manconi R, Sarà A, Sidri M, Pronzato R. The marine sponge chondrilla nucula schmidt, 1862 as an elective candidate for bioremediation in integrated aquaculture. Biomol Eng. 2003;20:363–8.

    Article  CAS  PubMed  Google Scholar 

  174. Stabilia L, Liccianoa M, Giangrandea A, Longoc C, Mercurioc M, Marzanoc CN, et al. Filtering activity of Spongia officinalis var. adriatica (schmidt) (Porifera, Demospongiae) on bacterioplankton: implications for bioremediation of polluted seawater. Water Res. 2006;40:3083–90.

    Article  CAS  Google Scholar 

  175. Xue L, Zhang X, Zhang W. Larval release and settlement of the marine sponge Hymeniacidon perlevis (Porifera, Demospongiae) under controlled laboratory conditions. Aquaculture. 2009;290:132–9.

    Article  Google Scholar 

  176. de Voogd NJ, Cleary DFR, Polónia ARM, Gomes NCM. Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, west java, Indonesia. FEMS Microbiol Ecol. 2015;91:1–12.

    Article  CAS  Google Scholar 

  177. Webster NS. Sponge disease: a global threst? Environ Microbiol. 2007;9:1363–75.

    Article  CAS  PubMed  Google Scholar 

  178. Gaino E, Pronzato R, Corriero G, Buffa P. Mortality of commercial sponges: incidence in two mediterranean areas. Ital J Zool. 1992;59:79–85.

    Google Scholar 

  179. Gaino E, Pronzato R. Epidemie e pesca intensive minacciano la sopravvirenza delle spugne commeciali del bacino mediterraneo. Bollettino dei Musei e degli Istituti Biologici dell’Universita di Genova. 1992;56:209–24.

    Google Scholar 

  180. Vacelet J. The struggle against the epidemic which is decimating mediterranean sponges. Technical report. Rome; 1994, FI:TCP/RAB/8853.

    Google Scholar 

  181. Castritsi-Catharios J, Kefalas E. Spreading of the sponge disease in the eastern mediterranean. In: 2nd workshop on sponge disease ‘Mass mortality of mediterranean sponges’. University of Genova, Italy; 1999.

    Google Scholar 

  182. Fang JKH, Mello-Athayde MA, Schönberg CHL, Kline DI, Hoegh-Guldberg O, Dove S. Sponge biomass and bioerosion rates increase under ocean warming and acidification. Glob Chang Biol. 2013;19:3581–91.

    Article  PubMed  Google Scholar 

  183. Webster N, Pantile R, Botté E, Abdo D, Andreakis N, Whalan S. A complex life cycle in a warming planet: gene expression in thermally stressed sponges. Mol Ecol. 2013;22:1854–68.

    Article  CAS  PubMed  Google Scholar 

  184. Angermeier H, Glöckner V, Pawlik JR, Lindquist NL, Hentschel U. Sponge white patch disease affecting the caribbean sponge Amphimedon compressa. Dis Aquat Org. 2012;99:95–102.

    Article  CAS  Google Scholar 

  185. Negri AP, Soo RM, Flores F, Webster NS. Bacillus insecticides are not acutely harmful to corals and sponges. Mar Ecol Prog Ser. 2009;381:157–65.

    Article  CAS  Google Scholar 

  186. Luter HM, Whalan S, Webster NS. Prevalence of tissue necrosis and brown spot lesions in a common marine sponge. Mar Freshw Res. 2010;61:484–9.

    Article  Google Scholar 

  187. Angermeier H, Kamke J, Abdelmohsen UR, Krohne G, Pawlik JR, Lindquist NL, et al. The pathology of sponge orange band disease affecting the caribbean barrel sponge Xestospongia muta. FEMS Microbiol Ecol. 2011;75:218–30.

    Article  CAS  PubMed  Google Scholar 

  188. Galstoff PS. Wasting disease causing mortality of sponges in the west indies and gulf of Mexico. Proc VIII Am Sci Congr. 1942;3:411–21.

    Google Scholar 

  189. Gammill ER, Fenner D. Disease threatens caribbean sponges: report and identification guide. ReefBase: A Global Information System for Coral Reefs; 2005. Available at http://www.reefbase.org/spongedisease/

  190. Luter HM, Whalan S, Webster NS. Thermal and sedimentation stress are unlikely causes of brown spot syndrome in the coral reef sponge, Ianthella basta. PLoS One. 2012;7:e39779.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Webster NS, Negri AP, Webb RI, Hill RT. A spongin-boring α-proteobacterium is the etiological agent of disease in the great barrier reef sponge Rhopaloeides odorabile. Mar Ecol Prog Ser. 2002;232:305–9.

    Article  Google Scholar 

  192. Brock TD. Milestones in microbiology. Englewood Cliffs: Prentice Hall; 1961.

    Google Scholar 

  193. Mukherjee J, Webster N, Llewellyn LE. Purification and characterization of a collagenolytic enzyme from a pathogen of the great barrier reef sponge, Rhopaloeides odorabile. PLoS One. 2009;4:e7177.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  194. Choudhury JD, Pramanik A, Webster NS, Llewellyn LE, Gachhui R, Mukherjeea J. Draft genome sequence of Pseudoalteromonas sp. Strain nw 4327 (MTCC 11073, DSM 25418), a pathogen of the great barrier reef sponge Rhopaloeides odorabile. Genome Announc. 2014;2:e00001–14.

    Article  PubMed  PubMed Central  Google Scholar 

  195. Choudhury JD, Pramanik A, Webster NS, Llewellyn LE, Gachhui R, Mukherjee J. The pathogen of the great barrier reef sponge Rhopaloeides odorabile is a new strain of Pseudoalteromonas agarivorans containing abundant and diverse virulence-related genes. Mar Biotechnol. 2015;17:463–78.

    Article  CAS  Google Scholar 

  196. Sweet M, Bulling M, Cerrano C. A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs. 2015;34:871–83.

    Article  Google Scholar 

  197. Rützler K. Mangrove sponge disease induced by cyanobacterial symbionts: failure of a primitive immune system? Dis Aquat Org. 1988;5:143–9.

    Article  Google Scholar 

  198. Butler MJ, Hunt JH, Herrnkind WF, Childress MJ, Bertelsen R, Sharp W. Cascading disturbances in florida bay, USA: cyanobacteria blooms, sponge mortality, and implications for juvenile spiny lobsters panulirus argus. Mar Ecol Prog Ser. 1995;129:119–25.

    Article  Google Scholar 

  199. Vacelet J, Gallissian M-F. Virus-like particles in cells of the sponge Verongia cavernicola (Demospongiae, Dictyoceratida) and accompanying tissue changes. J Invertebr Pathol. 1978;31:246–54.

    Article  Google Scholar 

  200. Olson JB, Gochfeld DJ, Slattery M. Aplysina red band syndrome: a new threat to caribbean sponges. Dis Aquat Org. 2006;72:163–8.

    Article  Google Scholar 

  201. Gochfeld DJ, Schlöder C, Thacker RW. Sponge community structure and disease prevalence on coral reefs in Bocas del Toro, Panama. In: Custódio MR, Lôbo-Hajdu G, Hajdu E, Muricy G, editors. Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro: Série Livros, Museu Nacional; 2007. p. 335–44.

    Google Scholar 

  202. Easson CG, Slattery M, Momm HG, Olson JB, Thacker RW, Gochfeld DJ. Exploring individual- to population-level impacts of disease on coral reef sponges: using spatial analysis to assess the fate, dynamics, and transmission of Aplysina red band syndrome (ARBS). PLoS One. 2013;8:e79976.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  203. Cowart JD, Henkel TP, McMurray SE, Pawlik JR. Sponge orange band (SOB): a pathogenic-like condition of the giant barrel sponge Xestospongia muta. Coral Reefs. 2006;25:513.

    Article  Google Scholar 

  204. Stevely JM, Sweat DE, Bert TM, Sim-Smith C, Kelly M. Sponge mortality at Marathon and Long key, Florida: patterns of species response and population recovery. Proceeding of the 63rd Gulf and Caribbean Fisheries Institute. San Juan, Puerto Rico; 2011. p. 384–400.

    Google Scholar 

  205. Luter HM, Whalan S, Webster NS. The marine sponge Ianthella basta can recover from stress-induced tissue regression. Hydrobiologia. 2012;687:227–35.

    Article  Google Scholar 

  206. Di Camillo CG, Bartolucci I, Cerrano C, Bavestrello G. Sponge disease in the adriatic sea. Mar Ecol. 2013;34:62–7.

    Article  Google Scholar 

  207. Carter HJ. Parasites of the spongida. Ann Mag Nat Hist. 1878;2:157–72.

    Article  Google Scholar 

  208. Brice JJ. The fish and fisheries of the coastal waters of Florida. US Bur Fish Rept Comm Fish. 1896;22:263–342.

    Google Scholar 

  209. Allemand-Martin A. Étude de physiologie appliquÉe sur la spongiculture sur le côtes de tunisie. In: Lyon; 1906.

    Google Scholar 

  210. Allemand-Martin A. Contribution à l’Étude de la culture des Éponges. Cr Ass Advmt Sci Tunis. 1914;42:375–7.

    Google Scholar 

  211. Storr JF. Ecology of the gulf of Mexico commercial sponges and its relation to the fishery. US Fish Wildl Serv Spec Scient Rep. 1964;466:1–73.

    Google Scholar 

  212. Galstoff PS, Brown HH, Smith CL, Walton Smith FG. Sponge mortality in the Bahamas. Nature. 1939;143:807–8.

    Article  Google Scholar 

  213. Smith FGW. Sponge disease in British Honduras, and its transmission by water currents. Ecology. 1941;22:415–21.

    Article  Google Scholar 

  214. Smith FGW. Sponge mortality at British Honduras. Nature. 1939;143:785.

    Article  Google Scholar 

  215. Stachowitsch M. Mass mortality in gulf of Trieste: the course of community destruction. Mar Ecol. 1984;5:243–64.

    Article  Google Scholar 

  216. Wulff JL. Sponge systematics by starfish: predators distinguish cryptic sympatric species of caribbean fire sponges, Tedania ignis and Tedania klausi n. sp. (Demospongiae, Poecilosclerida). Biol Bull. 2006;211:83–94.

    Article  PubMed  Google Scholar 

  217. Wulff JL. Ecological interactions of marine sponges. Can J Zool. 2006;84:146–66.

    Article  Google Scholar 

  218. Economou E, Konteatis D. Information on the sponge disease of 1986 in the waters of cyprus. Report of department of fisheries, ministry of agriculture and natural resources. Republic of Cyprus, Ministry of Agriculture and Natural Resources, Cyprus; 1988.

    Google Scholar 

  219. Rizzello R, Corriero G, Scalera-Liaci L, Pronzato R. Extinction and recolonization of spongia officinalis in the Marsala lagoon. Biol Mar Mediterr. 1997;4:443–4.

    Google Scholar 

  220. Gashout SF, Haddud DA, El-Zintani AA, Elbare RMA. Evidence for infection of libyan sponge grounds. In: International seminar on the combat of pollution and the conservation of marine wealth in the Mediterranean sea. Gulf of Sirte: Marine Biological Resources Centre; 1989. p. 100–13.

    Google Scholar 

  221. Turon X, Tarjuelo I, Uriz MJ. Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: correlation with population structure and investment in defence. Funct Ecol. 1998;12:631–9.

    Article  Google Scholar 

  222. Corriero G, Scalera-Liaci L, Rizzello R. Osservazioni sulla mortalita Diircinia spinosula (schmidt) and Ircinia sp. (Porifera, Demospongiae) nell′ insenatura della strea di porto cesareo. Thalassia Salent. 1996;22:51–62.

    Google Scholar 

  223. Paz M. New killer disease attacks giant barrel sponge; 1997. Available at: http://sanpedrosun.net/old/sponge.html

  224. Cervino JM, Winiarski-Cervino K, Polson SW, Goreau T, Smith GW. Identification of bacteria associated with a disease affecting the marine sponge Ianthella basta in New Britain, Papua New Guinea. Mar Ecol Prog Ser. 2006;324:139–50.

    Article  CAS  Google Scholar 

  225. Nagelkerken I, Aerts L, Pros LPJJ. Barrel sponge bows out. Reef Encounter. 2000;28:14–5.

    Google Scholar 

  226. Cerrano C, Magnino G, Sarà A, Bavestrello G, Gaino E. Necrosis in a population of Petrosia ficiformis (Porifera, Demospongiae) in relation with environmental stress. Ital J Zool. 2001;68:131–6.

    Article  Google Scholar 

  227. Wulff JL. A simple model of growth form-dependent recovery from disease in coral reef sponges, and implications for monitoring. Coral Reefs. 2006;25:419–26.

    Article  Google Scholar 

  228. Wulff JL. Disease prevalence and population density over time in three common caribbean coral reef sponge species. J Mar Biol Assoc UK. 2007;87:1715–20.

    Article  Google Scholar 

  229. Cerrano C, Bavestrello G, Bianchi CK, Cattaneo-vietti R, Bava S, Morganti C, et al. A catastrophic mass-mortality episode of gorgonians and other organisms in the ligurian sea (north-western mediterranean), summer 1999. Ecol Lett. 2000;3:284–93.

    Article  Google Scholar 

  230. Böhm M, Hentschel U, Friedrich AB, Fiesler L, Steffen R, Gamulin V, et al. Molecular response of the sponge suberites domuncula to bacterial infection. Mar Biol. 2001;139:1037–45.

    Article  CAS  Google Scholar 

  231. Skoufas G. Massive necrosis of sedentary benthic animal organisms in the north aegean sea. 7th Hellenic symposium on oceanography and fisheries. Chersonissos: National Centre for Marine Research; 2003.

    Google Scholar 

  232. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, et al. Mass mortality in northwestern mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol. 2009;15:1090–103.

    Article  Google Scholar 

  233. Castritsi-Catharios J, Miliou H, Kapiris K, Kefalas E. Recovery of the commercial sponges in the central and southeastern aegean sea (NE Mediterranean) after an outbreak of sponge disease. Mediterr Mar Sci. 2011;12:5–20.

    Article  Google Scholar 

  234. Di Camillo CG, Cerrano C. Mass mortality events in the NW Adriatic Sea: phase shift from slow- to fast-growing organisms. PLoS One. 2015;10:e0126689.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  235. Cerrano C, Bavestrello G. Mass mortalities and extinctions. In: Wahl M, editor. Marine hard bottom communities ecological studies 206. Berlin/Heidelberg: Springer; 2009. p. 295–307.

    Chapter  Google Scholar 

  236. Diaz MC, Ruetzler K. Sponges: an essential component of caribbean coral reefs. Bull Mar Sci. 2001;69:535–46.

    Google Scholar 

  237. Wulff J. Assessing and monitoring coral reef sponges: why and how? Bull Mar Sci. 2001;69:831–46.

    Google Scholar 

  238. Hayes RL, Goreau NI. The significance of emerging diseases in the tropical coral reef ecosystem. Rev Biol Trop. 1998;5:173–85.

    Google Scholar 

  239. Goreau TJ, Cervino J, Goreau M, Hayes R, Hayes M, Richardson L. Rapid spread of diseases in caribbean coral reefs. Rev Biol Trop. 1998;46:157–71.

    Google Scholar 

  240. Williams JEH, Bunkley-Williams L. Marine major ecological disturbances of the Caribbean. J Infect Dis Rev. 2000;2:110–27.

    Google Scholar 

  241. Reiswig HM. Population dynamics of three jamaican demospongiae. Bull Mar Sci. 1973;23:191–226.

    Google Scholar 

  242. Hummel H, Sepers ABJ, de Wolf L, Melissen FW. Bacterial growth on the marine sponge Halichondria panicea induced by reduced waterflow rate. Mar Ecol Prog Ser. 1988;42:195–8.

    Article  Google Scholar 

  243. Fedra K, Ölscher EM, Scherübel C, Stachowitsch M, Wurzian RS. On the ecology of a north adriatic benthic community: distribution, standing crop and composition of the macrobenthos. Mar Biol. 1976;38:129–45.

    Article  Google Scholar 

  244. Stachowitsch M. Anoxia in the northern adriatic sea: rapid death, slow recovery. In: Tyson RV, Pearson TH, editors. Modern and ancient continental shelf anoxia. London: Geological Society, Special Publications; 1991. p. 119–29.

    Google Scholar 

  245. Zocchi E, Basile G, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, et al. Aba- and cadpr-mediated effects on respiration and filtration downstream of the temperature-signaling cascade in sponges. J Cell Sci. 2003;116:629–36.

    Article  CAS  PubMed  Google Scholar 

  246. Previati M, Scinto A, Cerrano C, Osinga R. Oxygen consumption in mediterranean octocorals under different temperatures. J Exp Mar Biol Ecol. 2010;390:39–48.

    Article  Google Scholar 

  247. Bavestrello G, Puce S, Cerrano C, Zocchi E, Boero N. The problem of seasonality of benthic hydroids in temperate waters. Chem Ecol. 2006;22:197–205.

    Article  CAS  Google Scholar 

  248. Vezzulli L, Previati M, Pruzzo C, Marchese A, Bourne DG, Cerrano C, et al. Vibrio infections triggering mass mortality events in a warming mediterranean sea. Environ Microbiol. 2010;12:2007–9.

    Article  CAS  PubMed  Google Scholar 

  249. Torrents O, Tambutté E, Caminiti N, Garrabou J. Upper thermal thresholds of shallow vs. deep populations of the precious mediterranean red coral Corallium rubrum (l.): assessing the potential effects of warming in the nw mediterranean. J Exp Mar Biol Ecol. 2008;357:7–19.

    Article  Google Scholar 

  250. Kelly-Borges M, Bergquist PR. Sponges from motupore island, Papua New Guinea. Indo-Malayan Zool. 1988;5:121–59.

    Google Scholar 

  251. Vincente VP. An ecological evaluation of the west indian demosponge Anthosigmella varians (Hadromerida, Spriastrellidae). Bull Mar Sci. 1978;28:771–7.

    Google Scholar 

  252. Pronzato R. Sponge-fishing, disease and farming in the mediterranean sea. Aquat Conserv Mar Freshwat Ecosyst. 1999;9:485–93.

    Article  Google Scholar 

  253. Castritsi-catharios J, Miliou H, Pantelis J. Experimental sponge fishery in Egypt during recovery from sponge disease. Aquat Conserv Mar Freshwat Ecosyst. 2005;15:109–16.

    Article  Google Scholar 

  254. Corriero G, Longo C, Mercurio M, Marzano CN, Lembo G, Spedicato MT. Rearing performance of Spongia officinalis on suspended ropes off the southern italian coast (Central Mediterranean Sea). Aquaculture. 2004;238:195–205.

    Article  Google Scholar 

  255. Rützler K, Smith KP. Guide to the Western Atlantic species of Cinachyrella (Porifera: Tetillidae). In: Proceedings of the biological Society of Washington; 1992.

    Google Scholar 

  256. Butler MJI. Algae bloom impacts on hard bottom communities. In: Donahue S, editor. Algae bloom workshop: re-evaluation of management needs in Florida Bay. Key West: Florida Keys National Marine Sanctuary Program; 2008. p. 10–1.

    Google Scholar 

  257. Wulff J. Regeneration of sponges in ecological context: is regeneration an integral part of life history and morphological strategies? Integr Comp Biol. 2010;50:494–505.

    Article  PubMed  Google Scholar 

  258. Waddell B, Pawlik JR. Defenses of caribbean sponges against invertebrate predators. I. Assays with hermit crabs. Mar Ecol Prog Ser. 2000;195:125–32.

    Article  Google Scholar 

  259. Walters KD, Pawlik JR. Is there a trade-off between wound-healing and chemical defenses among caribbean reef sponges? Integr Comp Biol. 2005;45:352–8.

    Article  PubMed  Google Scholar 

  260. Leong W, Pawlik JR. Fragments or propagules? Reproductive tradeoffs among Callyspongia spp. from Florida coral reefs. Oikos. 2009;119:1417–22.

    Article  Google Scholar 

  261. DeBiasse MB, Richards VP, Shivji MS. Genetic assessment of connectivity in the common reef sponge, Callyspongia vaginalis (Demospongiae: Haplosclerida) reveals high population structure along the Florida reef tract. Coral Reefs. 2010;29:47–55.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Marine Drugs, State Key Laboratory of Oncogene and Related Genes, Department of Pharmacy, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China

    Qi Yang & Wei Zhang

  2. Centre for Marine Bioproducts Development, Flinders University, Adelaide, South Australia, Australia

    Qi Yang, Wei Zhang & Christopher M. M. Franco

  3. Medical Biotechnology, College of Medicine and Public Health, Flinders University, Adelaide, South Australia, Australia

    Qi Yang, Wei Zhang & Christopher M. M. Franco

Authors
  1. Qi Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher M. M. Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Zhang .

Editor information

Editors and Affiliations

  1. Marine Biotechnology Laboratory, State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China

    Zhiyong Li

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature B.V.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yang, Q., Zhang, W., Franco, C.M.M. (2019). Response of Sponge Microbiomes to Environmental Variations. In: Li, Z. (eds) Symbiotic Microbiomes of Coral Reefs Sponges and Corals. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-1612-1_11

Download citation

Publish with us

Policies and ethics

Search

Navigation