Advertisement

BluePharmTrain: Biology and Biotechnology of Marine Sponges

  • Georg Steinert
  • Carla Huete Stauffer
  • Nele Aas-Valleriani
  • Erik Borchert
  • Agneya Bhushan
  • Alexandra Campbell
  • Maryam Chaib De Mares
  • Margarida Costa
  • Johanna Gutleben
  • Stephen Knobloch
  • Robert Gregory Lee
  • Stephanie Munroe
  • Deepak Naik
  • Eike Edzard Peters
  • Ellen Stokes
  • Wanlin Wang
  • Eydís Einarsdóttir
  • Detmer Sipkema
Chapter
Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)

Abstract

BluePharmTrain is a Marie Curie Initial Training Network of 17 European academic and industrial partners collaborating to train young scientists in multidisciplinary aspects of blue biotechnology. Harvesting marine sponges for the extraction of bioactive compounds is often highly unsustainable, and the chemical synthesis of promising compounds is often either too complex or very expensive. To find sustainable and economically feasible production methods of sponge-derived compounds, individual BluePharmTrain research projects explore innovative techniques, focusing on selected sponge species shown to harbour interesting active metabolites. The different techniques include sponge cell cultivation, cultivation of microbial symbionts, next-generation sequencing approaches (i.e. metagenomics and metatranscriptomics), in situ and ex situ cultivation of sponges, life cycle characterisation, chemical structure elucidation of compounds and compound metabolic pathway description. Altogether, these consorted efforts and collaborations lead to new insights on sponge metabolism, sponge-microbe interactions and bioactive compound production.

References

  1. 1.
    Blunt JW, Copp BR, Keyzers RA et al (2016) Marine natural products. Nat Prod Rep 33:382–431.  https://doi.org/10.1039/C5NP00156K CrossRefGoogle Scholar
  2. 2.
    Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347.  https://doi.org/10.1128/MMBR.00040-06 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Maldonado M (2007) Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically-compartmented bacterial types. J Mar Biol Assoc UK 87:1701–1713.  https://doi.org/10.1017/S0025315407058080 CrossRefGoogle Scholar
  4. 4.
    Ahn YB, Kerkhof LJ, Häggblom MM (2009) Desulfoluna spongiiphila sp. nov., a dehalogenating bacterium in the Desulfobacteraceae from the marine sponge Aplysina aerophoba. Int J Syst Evol Microbiol 59:2133–2139.  https://doi.org/10.1099/ijs.0.005884-0 CrossRefPubMedGoogle Scholar
  5. 5.
    Gazave E, Lapébie P, Ereskovsky AV et al (2011) No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia 687:3–10.  https://doi.org/10.1007/s10750-011-0842-x CrossRefGoogle Scholar
  6. 6.
    Morrow C, Cárdenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front Zool 12:7.  https://doi.org/10.1186/s12983-015-0099-8 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Van Soest RWM, Boury-Esnault N, Hooper JNA, et al (2017) World Porifera database. http://www.marinespecies.org/porifera
  8. 8.
    Conway Morris S (1998) Early metazoan evolution: reconciling paleontology and molecular biology. Am Zool 38:867–877.  https://doi.org/10.1093/icb/38.6.867 CrossRefGoogle Scholar
  9. 9.
    Dewel RA (2000) Colonial origin for eumetazoa: major morphological transitions and the origin of bilaterian complexity. J Morphol 243:35–74CrossRefGoogle Scholar
  10. 10.
    Halanych KM (2015) The ctenophore lineage is older than sponges? That cannot be right! Or can it? J Exp Biol 218:592–597.  https://doi.org/10.1242/jeb.111872 CrossRefPubMedGoogle Scholar
  11. 11.
    Ryan JF, Pang K, Schnitzler CE et al (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:1242592.  https://doi.org/10.1126/science.1242592 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Yin Z, Zhu M, Davidson EH et al (2015) Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci U S A 112:201414577.  https://doi.org/10.1073/pnas.1414577112 CrossRefGoogle Scholar
  13. 13.
    Ayling AL (1980) Patterns of sexuality, asexual reproduction and recruitment in some subtidal marine demosponge. Biol Bull 158:271–282.  https://doi.org/10.2307/1540854 CrossRefGoogle Scholar
  14. 14.
    Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654.  https://doi.org/10.1038/nrmicro2839 CrossRefPubMedGoogle Scholar
  15. 15.
    Wehrl M, Steinert M, Hentschel U (2007) Bacterial uptake by the marine sponge Aplysina aerophoba. Microb Ecol 53:355–365.  https://doi.org/10.1007/s00248-006-9090-4 CrossRefPubMedGoogle Scholar
  16. 16.
    Borchiellini C, Manuel M, Alivon E et al (2001) Sponge paraphyly and the origin of Metazoa. J Evol Biol 14:171–179.  https://doi.org/10.1046/j.1420-9101.2001.00244.x CrossRefPubMedGoogle Scholar
  17. 17.
    Halanych KM (2004) The new view of animal phylogeny. Annu Rev Ecol Evol Syst 35:229–256.  https://doi.org/10.1146/annurev.ecolsys.35.112202.130124 CrossRefGoogle Scholar
  18. 18.
    Li C (1998) Precambrian sponges with cellular structures. Science 279:879–882.  https://doi.org/10.1126/science.279.5352.879 CrossRefPubMedGoogle Scholar
  19. 19.
    Wilkinson CR (1984) Immunological evidence for the precambrian origin of bacterial symbioses in marine sponges. Proc R Soc Lond 220:509–518.  https://doi.org/10.1098/rspb.1984.0017 CrossRefGoogle Scholar
  20. 20.
    Reveillaud J, Maignien L, Eren MA et al (2014) Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8:1198–1209.  https://doi.org/10.1038/ismej.2013.227 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Thomas T, Moitinho-Silva L, Lurgi M et al (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870.  https://doi.org/10.1038/ncomms11870 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Ribes M, Coma R, Gili JM (1999) Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Mar Ecol Prog Ser 176:179–190.  https://doi.org/10.3354/meps176179 CrossRefGoogle Scholar
  23. 23.
    Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30:301–314CrossRefGoogle Scholar
  24. 24.
    Wilkinson CR (1978) Microbial associations in sponges. I. Ecology, physiology and microbial populations of coral reef sponges. Mar Biol 49:161–167.  https://doi.org/10.1007/BF00387115 CrossRefGoogle Scholar
  25. 25.
    Wilkinson CR (1978) Microbial associations in sponges. II. Numerical analysis of sponge and water bacterial populations. Mar Biol 49:169–176.  https://doi.org/10.1007/BF00387116 CrossRefGoogle Scholar
  26. 26.
    Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177.  https://doi.org/10.1111/j.1574-6941.2005.00046.x CrossRefPubMedGoogle Scholar
  27. 27.
    Reiswig HM (1981) Partial carbon and energy budgets of the bacteriosponge Verohgia fistularis (Porifera: Demospongiae) in Barbados. Mar Ecol 2:273–293.  https://doi.org/10.1111/j.1439-0485.1981.tb00271.x CrossRefGoogle Scholar
  28. 28.
    Abdelmohsen UR, Bayer K, Hentschel U (2014) Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat Prod Rep 31:381–399.  https://doi.org/10.1039/c3np70111e CrossRefPubMedGoogle Scholar
  29. 29.
    Bayer K, Kamke J, Hentschel U (2014) Quantification of bacterial and archaeal symbionts in high and low microbial abundance sponges using real-time PCR. FEMS Microbiol Ecol 89:679–690.  https://doi.org/10.1111/1574-6941.12369 CrossRefPubMedGoogle Scholar
  30. 30.
    Moitinho-Silva L, Bayer K, Cannistraci CV et al (2014) Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea. Mol Ecol 23:1348–1363.  https://doi.org/10.1111/mec.12365 CrossRefPubMedGoogle Scholar
  31. 31.
    Noyer C, Hamilton A, Sacristan-Soriano O, Becerro MA (2010) Quantitative comparison of bacterial communities in two Mediterranean sponges. Symbiosis 51:239–243.  https://doi.org/10.1007/s13199-010-0082-2 CrossRefGoogle Scholar
  32. 32.
    Gloeckner V, Wehrl M, Moitinho-Silva L et al (2014) The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull 227:78–88CrossRefGoogle Scholar
  33. 33.
    Hentschel U, Hopke J, Horn M et al (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440.  https://doi.org/10.1128/AEM.68.9.4431-4440.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Simister RL, Deines P, Botté ES et al (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14:517–524.  https://doi.org/10.1111/j.1462-2920.2011.02664.x CrossRefPubMedGoogle Scholar
  35. 35.
    Taylor MW, Tsai P, Simister RL et al (2013) “Sponge-specific” bacteria are widespread (but rare) in diverse marine environments. ISME J 7:438–443.  https://doi.org/10.1038/ismej.2012.111 CrossRefPubMedGoogle Scholar
  36. 36.
    Taylor MW, Schupp PJ, Dahllöf I et al (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130.  https://doi.org/10.1046/j.1462-2920.2003.00545.x CrossRefPubMedGoogle Scholar
  37. 37.
    Webster NS, Taylor MW, Behnam F et al (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070–2082.  https://doi.org/10.1111/j.1462-2920.2009.02065.x CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Wilkinson CR (1978) Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Mar Biol 49:177–185.  https://doi.org/10.1007/BF00387117 CrossRefGoogle Scholar
  39. 39.
    Easson CG, Thacker RW (2014) Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front Microbiol 5:1–11.  https://doi.org/10.3389/fmicb.2014.00532 CrossRefGoogle Scholar
  40. 40.
    Pita L, Turon X, López-Legentil S, Erwin PM (2013) Host rules: spatial stability of bacterial communities associated with marine sponges (Ircinia spp.) in the Western Mediterranean Sea. FEMS Microbiol Ecol 86:268–276.  https://doi.org/10.1111/1574-6941.12159 CrossRefPubMedGoogle Scholar
  41. 41.
    Steinert G, Taylor MW, Deines P et al (2016) In four shallow and mesophotic tropical reef sponges from Guam the microbial community largely depends on host identity. PeerJ 4:e1936.  https://doi.org/10.7717/peerj.1936 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Erwin PM, Thacker RW (2008) Phototrophic nutrition and symbiont diversity of two Caribbean sponge-cyanobacteria symbioses. Mar Ecol Prog Ser 362:139–147.  https://doi.org/10.3354/meps07464 CrossRefGoogle Scholar
  43. 43.
    Lee OO, Chui PY, Wong YH et al (2009) Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microbiol 75:6147–6156.  https://doi.org/10.1128/AEM.00023-09 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Schmitt S, Angermeier H, Schiller R et al (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microbiol 74:7694–7708.  https://doi.org/10.1128/AEM.00878-08 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Schmitt S, Weisz JB, Lindquist N, Hentschel U (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microbiol 73:2067–2078.  https://doi.org/10.1128/AEM.01944-06 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Sharp KH, Eam B, John Faulkner D, Haygood MG (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73:622–629.  https://doi.org/10.1128/AEM.01493-06 CrossRefPubMedGoogle Scholar
  47. 47.
    Uriz MJ, Agell G, Blanquer A et al (2012) Endosymbiotic calcifying bacteria: a new cue to the origin of calcification in metazoa? Evolution (NY) 66:2993–2999.  https://doi.org/10.1111/j.1558-5646.2012.01676.x CrossRefGoogle Scholar
  48. 48.
    Uriz MJ, Turon X, Becerro MA (2001) Morphology and ultrastructure of the swimming larvae of Crambe crambe (Demospongiae, Poecilosclerida). Invertebr Biol 120:295–307CrossRefGoogle Scholar
  49. 49.
    Usher KM, Sutton DC, Toze S et al (2005) Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Mar Freshw Res 56:125–131.  https://doi.org/10.1071/MF04304 CrossRefGoogle Scholar
  50. 50.
    Schmitt S, Tsai P, Bell J et al (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576CrossRefGoogle Scholar
  51. 51.
    Thacker RW, Freeman CJ (2012) Sponge–microbe symbioses. Adv Mar Biol 62:57–111CrossRefGoogle Scholar
  52. 52.
    Sipkema D, de Caralt S, Morillo JA et al (2015) Similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission. Environ Microbiol.  https://doi.org/10.1111/1462-2920.12827
  53. 53.
    de Goeij JM, van Oevelen D, Vermeij MJA et al (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110.  https://doi.org/10.1126/science.1241981 CrossRefPubMedGoogle Scholar
  54. 54.
    Rix L, de Goeij JM, Mueller CE et al (2016) Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems. Sci Rep 6:18715.  https://doi.org/10.1038/srep18715 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546Google Scholar
  56. 56.
    Diaz MC, Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156:97–107.  https://doi.org/10.3354/meps156097 CrossRefGoogle Scholar
  57. 57.
    Hoffmann F, Radax R, Woebken D et al (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11:2228–2243.  https://doi.org/10.1111/j.1462-2920.2009.01944.x CrossRefPubMedGoogle Scholar
  58. 58.
    Schläppy ML, Schöttner SI, Lavik G et al (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157:593–602.  https://doi.org/10.1007/s00227-009-1344-5 CrossRefPubMedGoogle Scholar
  59. 59.
    Hoffmann F, Larsen O, Thiel V et al (2005) An anaerobic world in sponges. Geomicrobiol J 22:1–10.  https://doi.org/10.1080/01490450590922505 CrossRefGoogle Scholar
  60. 60.
    Fan L, Reynolds D, Liu M et al (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci U S A 109:E1878–E1887.  https://doi.org/10.1073/pnas.1203287109 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Hallam SJ, Konstantinidis KT, Putnam N et al (2006) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci U S A 103:18296–18301.  https://doi.org/10.1073/pnas.0608549103 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Liu M, Fan L, Zhong L et al (2012) Metaproteogenomic analysis of a community of sponge symbionts. ISME J 6:1515–1525.  https://doi.org/10.1038/ismej.2012.1 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Siegl A, Kamke J, Hochmuth T et al (2011) Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5:61–70.  https://doi.org/10.1038/ismej.2010.95 CrossRefGoogle Scholar
  64. 64.
    Freeman CJ, Thacker RW, Baker DM, Fogel ML (2013) Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? ISME J 7:1116–1125.  https://doi.org/10.1038/ismej.2013.7 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Freeman CJ, Easson CG, Baker DM (2014) Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras. Peer J 2:e695.  https://doi.org/10.7717/peerj.695 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Ribes M, Jiménez E, Yahel G et al (2012) Functional convergence of microbes associated with temperate marine sponges. Environ Microbiol 14:1224–1239.  https://doi.org/10.1111/j.1462-2920.2012.02701.x CrossRefPubMedGoogle Scholar
  67. 67.
    Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press, Cambridge, MAGoogle Scholar
  68. 68.
    Pita L, Fraune S, Hentschel U (2016) Emerging sponge models of animal-microbe symbioses. Front Microbiol 7:2102.  https://doi.org/10.3389/fmicb.2016.02102 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Bayer K, Scheuermayer M, Fieseler L, Hentschel U (2013) Genomic mining for novel FADH2-dependent halogenases in marine sponge-associated microbial consortia. Mar Biotechnol 15:63–72.  https://doi.org/10.1007/s10126-012-9455-2 CrossRefPubMedGoogle Scholar
  70. 70.
    Della Sala G, Hochmuth T, Costantino V et al (2013) Polyketide genes in the marine sponge Plakortis simplex: a new group of mono-modular type I polyketide synthases from sponge symbionts. Environ Microbiol Rep 5:809–818.  https://doi.org/10.1111/1758-2229.12081 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Thomas T, Rusch D, DeMaere MZ et al (2010) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4:1557–1567.  https://doi.org/10.1038/ismej.2010.74 CrossRefGoogle Scholar
  72. 72.
    Duckworth A (2009) Farming sponges to supply bioactive metabolites and bath sponges: a review. Mar Biotechnol (NY) 11:669–679.  https://doi.org/10.1007/s10126-009-9213-2 CrossRefGoogle Scholar
  73. 73.
    Brümmer F, Nickel M (2003) Sustainable use of marine resources: cultivation of sponges. In: Müller WEG (ed) Sponges (Porifera). Springer, Berlin, pp 143–162CrossRefGoogle Scholar
  74. 74.
    Pronzato R (2003) Mediterranean sponge fauna: a biological, historical and cultural heritage. Biogeographia 24:91–99CrossRefGoogle Scholar
  75. 75.
    Pronzato R, Manconi R (2008) Mediterranean commercial sponges: over 5000 years of natural history and cultural heritage. Mar Ecol 29:146–166.  https://doi.org/10.1111/j.1439-0485.2008.00235.x CrossRefGoogle Scholar
  76. 76.
    Stevely JM, Sweat DE, Bert TM et al (2010) Commercial bath sponge (Spongia and Hippospongia) and total sponge community abundance and biomass estimates in the Florida Middle and Upper Keys, USA Estimaciones de la Biomasa en los Cayos Central y Superior del Estado de Florida, EE. UU, de Espon. Proc Gulf Caribb Fish Inst 62:394–403Google Scholar
  77. 77.
    Vicente VP (1989) Regional commercial sponge extinctions in the west indies: are recent climatic changes responsible? Mar Ecol 10:179–191.  https://doi.org/10.1111/j.1439-0485.1989.tb00073.x CrossRefGoogle Scholar
  78. 78.
    Voultsiadou E, Vafidis D, Antoniadou C (2008) Sponges of economical interest in the Eastern Mediterranean: an assessment of diversity and population density. J Nat Hist 42:529–543.  https://doi.org/10.1080/00222930701835506 CrossRefGoogle Scholar
  79. 79.
    Duckworth AR, Wolff C (2007) Bath sponge aquaculture in Torres Strait, Australia: effect of explant size, farming method and the environment on culture success. Aquaculture 271:188–195.  https://doi.org/10.1016/j.aquaculture.2007.06.037 CrossRefGoogle Scholar
  80. 80.
    Wolff C (2004) Sponge farming in remote Australian communities. Australas Sci 25:35Google Scholar
  81. 81.
    Josupeit H (1990) Sponges: world production and markets. Food and Agriculture Organisation of the United Nations. FAO, SuvaGoogle Scholar
  82. 82.
    Voultsiadou E (2010) Therapeutic properties and uses of marine invertebrates in the ancient Greek world and early Byzantium. J Ethnopharmacol 130:237–247.  https://doi.org/10.1016/j.jep.2010.04.041 CrossRefPubMedGoogle Scholar
  83. 83.
    Sipkema D, Franssen MCR, Osinga R et al (2005) Marine sponges as pharmacy. Mar Biotechnol 7:142–162.  https://doi.org/10.1007/s10126-004-0405-5 CrossRefPubMedGoogle Scholar
  84. 84.
    Mehbub MF, Lei J, Franco C, Zhang W (2014) Marine sponge derived natural products between 2001 and 2010: trends and opportunities for discovery of bioactives. Mar Drugs 12:4539–4577.  https://doi.org/10.3390/md12084539 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Hirata Y, Uemura D (1986) Halichondrins – antitumor polyether macrolides from a marine sponge. Pure Appl Chem 58:701–710.  https://doi.org/10.1351/pac198658050701 CrossRefGoogle Scholar
  86. 86.
    Hayashi K, Hamada Y, Shioiri T (1992) Synthesis of nazumamide A, a thrombin-inhibitory linear tetrapeptide, from a marine sponge, Theonella sp. Tetrahedron Lett 33:5075–5076.  https://doi.org/10.1016/S0040-4039(00)61193-0 CrossRefGoogle Scholar
  87. 87.
    Sata NU, Matsunaga S, Fusetani N, Van Soest RWM (1999) Aurantosides D, E, and F: new antifungal tetramic acid glycosides from the marine sponge Siliquariaspongia japonica. J Nat Prod 62:969–971.  https://doi.org/10.1021/np9900021 CrossRefPubMedGoogle Scholar
  88. 88.
    Ferrandiz ML, Sanz MJ, Bustos G et al (1994) Avarol and avarone, 2 new antiinflammatory agents of marine origin. Eur J Pharmacol 253:75–82.  https://doi.org/10.1016/0014-2999(94)90759-5 CrossRefPubMedGoogle Scholar
  89. 89.
    Bucar F, Wube A, Schmid M (2013) Natural product isolation – how to get from biological material to pure compounds. Nat Prod Rep 30:525–545.  https://doi.org/10.1039/c3np20106f CrossRefPubMedGoogle Scholar
  90. 90.
    Quinn RJ (1988) Chemistry of aqueous marine extracts: isolation techniques. In: Scheuer PJ (ed) Bioorganic marine chemistry. Springer, Berlin, pp 1–41Google Scholar
  91. 91.
    Ankisetty S, Slattery M (2012) Antibacterial secondary metabolites from the cave sponge Xestospongia sp. Mar Drugs 10:1037–1043.  https://doi.org/10.3390/md10051037 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Roué M, Domart-Coulon I, Ereskovsky A et al (2010) Cellular localization of clathridimine, an antimicrobial 2-aminoimidazole alkaloid produced by the mediterranean calcareous sponge Clathrina clathrus. J Nat Prod 73:1277–1282.  https://doi.org/10.1021/np100175x CrossRefPubMedGoogle Scholar
  93. 93.
    Sauleau P, Moriou C, Al Mourabit A (2017) Metabolomics approach to chemical diversity of the Mediterranean marine sponge Agelas oroides. Nat Prod Res 6419:1–8.  https://doi.org/10.1080/14786419.2017.1285298 CrossRefGoogle Scholar
  94. 94.
    Di Bari G, Gentile E, Latronico T et al (2015) Inhibitory effect of aqueous extracts from marine sponges on the activity and expression of gelatinases A (MMP-2) and B (MMP-9) in rat astrocyte cultures. PLoS One 10(6):e0129322.  https://doi.org/10.1371/journal.pone.0129322 CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Sepčić K, Kauferstein S, Mebs D, Turk T (2010) Biological activities of aqueous and organic extracts from tropical marine sponges. Mar Drugs 8:1550–1566.  https://doi.org/10.3390/md8051550 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Pérez-Victoria I, Martín J, Reyes F (2016) Combined LC/UV/MS and NMR strategies for the dereplication of marine natural products. Planta Med 82:857–871.  https://doi.org/10.1055/s-0042-101763 CrossRefPubMedGoogle Scholar
  97. 97.
    Gaudencio SP, Pereira F (2015) Dereplication: racing to speed up the natural products discovery process. Nat Prod Rep 32:779–810.  https://doi.org/10.1039/c4np00134f CrossRefPubMedGoogle Scholar
  98. 98.
    Indraningrat AAG, Smidt H, Sipkema D (2016) Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar Drugs 14:87.  https://doi.org/10.3390/md14050087 CrossRefPubMedCentralGoogle Scholar
  99. 99.
    Youssef DTA, Shaala LA, Asfour HZ (2013) Bioactive compounds from the Red Sea marine sponge Hyrtios species. Mar Drugs 11:1061–1070.  https://doi.org/10.3390/md11041061 CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Cutignano A, Nuzzo G, Ianora A et al (2015) Development and application of a novel SPE-method for bioassay-guided fractionation of marine extracts. Mar Drugs 13:5736–5749.  https://doi.org/10.3390/md13095736 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Shaaban M, Abd-Alla HI, Hassan AZ et al (2012) Chemical characterization, antioxidant and inhibitory effects of some marine sponges against carbohydrate metabolizing enzymes. Org Med Chem Lett 2:30.  https://doi.org/10.1186/2191-2858-2-30\r2191-2858-2-30 CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Wolfender JL (2009) HPLC in natural product analysis: the detection issue. Planta Med 75:719–734.  https://doi.org/10.1055/s-0028-1088393 CrossRefPubMedGoogle Scholar
  103. 103.
    Li K, Chung-Davidson Y-W, Bussy U, Li W (2015) Recent advances and applications of experimental technologies in marine natural product research. Mar Drugs 13:2694–2713.  https://doi.org/10.3390/md13052694 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Bouslimani A, Sanchez LM, Garg N, Dorrestein PC (2014) Mass spectrometry of natural products: current, emerging and future technologies. Nat Prod Rep 31:718–729.  https://doi.org/10.1039/c4np00044g CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Breton RC, Reynolds WF (2013) Using NMR to identify and characterize natural products. Nat Prod Rep 30:501–524.  https://doi.org/10.1039/c2np20104f CrossRefPubMedGoogle Scholar
  106. 106.
    Kwan EE, Huang SG (2008) Structural elucidation with NMR spectroscopy: practical strategies for organic chemists. Eur J Org Chem:2671–2688.  https://doi.org/10.1002/ejoc.200700966 CrossRefGoogle Scholar
  107. 107.
    Riccio R, Bifulco G, Cimino P et al (2003) Stereochemical analysis of natural products. Approaches relying on the combination of NMR spectroscopy and computational methods. Pure Appl Chem 75:295–308.  https://doi.org/10.1351/pac200375020295 CrossRefGoogle Scholar
  108. 108.
    Blunt JW, Copp BR, Keyzers RA et al (2015) Marine natural products. Nat Prod Rep 32:116–211.  https://doi.org/10.1039/C4NP00144C CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Koopmans M, Martens D, Wijffels RH (2009) Towards commercial production of sponge medicines. Mar Drugs 7:787–802.  https://doi.org/10.3390/md7040787 CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Piel J (2004) Metabolites from symbiotic bacteria. Nat Prod Rep 21:519–538.  https://doi.org/10.1039/b310175b CrossRefPubMedGoogle Scholar
  111. 111.
    Wang G (2006) Diversity and biotechnological potential of the sponge-associated microbial consortia. J Ind Microbiol Biotechnol 33:545–551.  https://doi.org/10.1007/s10295-006-0123-2 CrossRefPubMedGoogle Scholar
  112. 112.
    Ebada SS, Lin W, Proksch P (2010) Bioactive sesterterpenes and triterpenes from marine sponges: occurrence and pharmacological significance. Mar Drugs 8:313–346.  https://doi.org/10.3390/md8020313 CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Gandhimathi R, Arunkumar M, Selvin J et al (2008) Antimicrobial potential of sponge associated marine actinomycetes. J Mycol Med 18:16–22.  https://doi.org/10.1016/j.mycmed.2007.11.001 CrossRefGoogle Scholar
  114. 114.
    Molinski TF, Dalisay DS, Lievens SL, Saludes JP (2009) Drug development from marine natural products. Nat Rev Drug Discov 8:69–85.  https://doi.org/10.1038/nrd2487 CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Sashidhara KV, White KN, Crews P (2009) A selective account of effective paradigms and significant outcomes in the discovery of inspirational marine natural products. J Nat Prod 72:588–603.  https://doi.org/10.1021/np800817y CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Bewley CA, Faulkner DJ (1998) Lithistid sponges: star performers or hosts to the stars. Angew Chem Int Ed 37:2162–2178CrossRefGoogle Scholar
  117. 117.
    Unson MD, Faulkner DJ (1993) Cyanobacterial symbiont biosynthesis of chlorinated metabolites from Dysidea herbacea (Porifera). Experientia 49:349–353.  https://doi.org/10.1007/BF01923420 CrossRefGoogle Scholar
  118. 118.
    Unson MD, Holland ND, Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of the crystalline metabolite in the sponge tissue. Mar Biol 119:1–11.  https://doi.org/10.1007/BF00350100 CrossRefGoogle Scholar
  119. 119.
    Narquizian R, Kocienski PJ (2000) The pederin family of antitumor agents: structures, synthesis and biological activity. In: Mulzer J, Bohlmann R (eds) The role of natural products in drug discovery. Springer, Berlin, pp 25–56CrossRefGoogle Scholar
  120. 120.
    Piel J, Butzke D, Fusetani N et al (2005) Exploring the chemistry of uncultivated bacterial symbionts: Antitumor polyketides of the Pederin family. J Nat Prod 68:472–479.  https://doi.org/10.1021/np049612d CrossRefPubMedGoogle Scholar
  121. 121.
    Kocienski P, Narquizian R, Raubo P et al (2000) Synthetic studies on the pederin family of antitumour agents. Syntheses of mycalamide B, theopederin D and pederin. J Chem Soc Perkin Trans 1(8):2357–2384.  https://doi.org/10.1039/a909898d CrossRefGoogle Scholar
  122. 122.
    Perry NB, Blunt JW, Munro MHG, Pannell LK (1988) Mycalamide A, an antiviral compound from a New Zealand sponge of the genus Mycale. J Am Chem Soc 110:4850–4851CrossRefGoogle Scholar
  123. 123.
    Sakemi S, Ichiba T, Kohmoto S et al (1988) Isolation and structure elucidation of onnamide A, a new bioactive metabolite of a marine sponge, Theonella sp. J Am Chem Soc 110:4851–4853CrossRefGoogle Scholar
  124. 124.
    Cichewicz RH, Valeriote FA, Crews P (2004) Psymberin, a potent sponge-derived cytotoxin from Psammocinia distantly related to the pederin family. Org Lett 6:1951–1954.  https://doi.org/10.1021/ol049503q CrossRefPubMedGoogle Scholar
  125. 125.
    Kampa A, Gagunashvili AN, Gulder T a M et al (2013) Metagenomic natural product discovery in lichen provides evidence for a family of biosynthetic pathways in diverse symbioses. Proc Natl Acad Sci U S A 110:E3129–E3137.  https://doi.org/10.1073/pnas.1305867110 CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Nakabachi A, Ueoka R, Oshima K et al (2013) Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol 23:1478–1484.  https://doi.org/10.1016/j.cub.2013.06.027 CrossRefPubMedGoogle Scholar
  127. 127.
    Wakimoto T, Egami Y, Nakashima Y et al (2014) Calyculin biogenesis from a pyrophosphate protoxin produced by a sponge symbiont. Nat Chem Biol 10:648–655.  https://doi.org/10.1038/nchembio.1573 CrossRefPubMedGoogle Scholar
  128. 128.
    Lackner G, Peters EE, Helfrich EJN, Piel J (2017) Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges. Proc Natl Acad Sci U S A 114:E347–E356.  https://doi.org/10.1073/pnas.1616234114 CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Uriz MJ, Turon X, Galera J, Tur JM (1996) New light on the cell location of avarol within the sponge Dysidea avara (Dendroceratida). Cell Tissue Res 285:519–527.  https://doi.org/10.1007/s004410050668 CrossRefGoogle Scholar
  130. 130.
    Andrade P, Willoughby R, Pomponi SA, Kerr RG (1999) Biosynthetic studies of the alkaloid, stevensine, in a cell culture of the marine sponge Teichaxinella morchella. Tetrahedron Lett 40:4775–4778.  https://doi.org/10.1016/S0040-4039(99)00881-3 CrossRefGoogle Scholar
  131. 131.
    Ternon E, Zarate L, Chenesseau S et al (2016) Spherulization as a process for the exudation of chemical cues by the encrusting sponge C. crambe. Sci Rep 6:29474.  https://doi.org/10.1038/srep29474 CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Turon X, Becerro MA, Uriz MJ (2000) Distribution of brominated compounds within the sponge Aplysina aerophoba: coupling of X-ray microanalysis with cryofixation techniques. Cell Tissue Res 301:311–322.  https://doi.org/10.1007/s004410000233 CrossRefPubMedGoogle Scholar
  133. 133.
    Lopp A, Reintamm T, Kuusksalu A et al (2012) A novel endoribonuclease from the marine sponge Tethya aurantium specific to 2',5'-phosphodiester bonds. Biochimie 94:1635–1646.  https://doi.org/10.1016/j.biochi.2012.04.002 CrossRefPubMedGoogle Scholar
  134. 134.
    Reintamm T, Lopp A, Kuusksalu A et al (2003) ATP N-glycosidase: a novel ATP-converting activity from a marine sponge Axinella polypoides. Eur J Biochem 270:4122–4132.  https://doi.org/10.1046/j.1432-1033.2003.03805.x CrossRefPubMedGoogle Scholar
  135. 135.
    Mendola D (2003) Aquaculture of three phyla of marine invertebrates to yield bioactive metabolites: process developments and economics. Biomol Eng 20:441–458.  https://doi.org/10.1016/S1389-0344(03)00075-3 CrossRefPubMedGoogle Scholar
  136. 136.
    Huyck TK, Gradishar W, Manuguid F, Kirkpatrick P (2011) Eribulin mesylate. Nat Rev Drug Discov 10:173–174.  https://doi.org/10.1038/nrd3389 CrossRefPubMedGoogle Scholar
  137. 137.
    Yu MJ, Zheng W, Seletsky BM (2013) From micrograms to grams: scale-up synthesis of eribulin mesylate. Nat Prod Rep 30:1158–1164.  https://doi.org/10.1039/c3np70051h CrossRefPubMedGoogle Scholar
  138. 138.
    Brand U, Görg C, Hirsch J, Wissen M (2008) Conflicts in environmental regulation and the internationalisation of the state: contested terrains. Routledge, LondonGoogle Scholar
  139. 139.
    Greiber T, Moreno SP, Ahrén M et al (2012) An explanatory guide to the Nagoya Protocol on access and benefit-sharing. IUCN, Gland, SwitzerlandGoogle Scholar
  140. 140.
    Laird S, Wynberg R (2012) Bioscience at a crossroads: implementing the Nagoya Protocol on access and benefit sharing in a time of scientific, technological and industry change. Secretariat of the Convention on Biological Diversity, Montréal, QCGoogle Scholar
  141. 141.
    Swanson TM (1998) The economics and ecology of biodiversity decline: the forces driving global change. Cambridge University Press, CambridgeGoogle Scholar
  142. 142.
    Richerzhagen C (2013) Protecting biological diversity: the effectiveness of access and benefit-sharing regimes. Routledge, New YorkGoogle Scholar
  143. 143.
    Battershill CN, Page MJ (1996) Sponge aquaculture for drug production. Aquac Updat 16:5–6Google Scholar
  144. 144.
    Osinga R, de Beukelaer PB, Meijer EM et al (1999a) Growth of the sponge Pseudosuberites (aff.) andrewsi in a closed system. J Biotechnol 70:155–161.  https://doi.org/10.1016/S0168-1656(99)00068-1 CrossRefGoogle Scholar
  145. 145.
    Verdenal B, Vacelet J (1990) Sponge culture on vertical ropes in the Northwestern Mediterranean Sea. In: Ruetzler K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, DC, pp 416–424Google Scholar
  146. 146.
    Belarbi EH, Contreras Gómez A, Chisti Y et al (2003) Producing drugs from marine sponges. Biotechnol Adv 21:585–598.  https://doi.org/10.1016/S0734-9750(03)00100-9 CrossRefGoogle Scholar
  147. 147.
    de Voogd NJ (2007) An assessment of sponge mariculture potential in the Spermonde Archipelago, Indonesia. J Mar Biol Assoc UK 87:1777–1784.  https://doi.org/10.1017/S0025315407057335 CrossRefGoogle Scholar
  148. 148.
    Duckworth A, Battershill C (2003) Sponge aquaculture for the production of biologically active metabolites: the influence of farming protocols and environment. Aquaculture 221:311–329.  https://doi.org/10.1016/S0044-8486(03)00070-X CrossRefGoogle Scholar
  149. 149.
    Muller WE, Wimmer W, Schatton W et al (1999) Initiation of an aquaculture of sponges for the sustainable production of bioactive metabolites in open systems: example, Geodia cydonium. Mar Biotechnol (NY) 1:569–579CrossRefGoogle Scholar
  150. 150.
    Ruiz C, Valderrama K, Zea S, Castellanos L (2013) Mariculture and natural production of the antitumoural (+)-discodermolide by the Caribbean marine sponge Discodermia dissoluta. Mar Biotechnol (NY) 15:571–583.  https://doi.org/10.1007/s10126-013-9510-7 CrossRefGoogle Scholar
  151. 151.
    van Treeck P, Eisinger M, Müller J et al (2003) Mariculture trials with Mediterranean sponge species: the exploitation of an old natural resource with sustainable and novel methods. Aquaculture 218:439–455.  https://doi.org/10.1016/S0044-8486(03)00010-3 CrossRefGoogle Scholar
  152. 152.
    Francis JC, Bart L, Poirrier MA (1990) Effect of medium pH on the growth rate of Ephydatia fluviatilis in laboratory culture. In: New perspectives in sponge biology. 3rd international sponge conference, pp 485–490Google Scholar
  153. 153.
    Hoffmann F, Rapp HT, Zoller T, Reitner J (2003) Growth and regeneration in cultivated fragments of the boreal deep water sponge Geodia barretti Bowerbank, 1858 (Geodiidae, Tetractinellida, Demospongiae). J Biotechnol 100:109–118CrossRefGoogle Scholar
  154. 154.
    Nickel M, Brummer F (2003) In vitro sponge fragment culture of Chondrosia reniformis (Nardo, 1847). J Biotechnol 100:147–159CrossRefGoogle Scholar
  155. 155.
    Osinga R, Tramper J, Wijffels RH (1998) Cultivation of marine sponges for metabolite production: applications for biotechnology? Trends Biotechnol 16:130–134.  https://doi.org/10.1016/S0167-7799(97)01164-5 CrossRefGoogle Scholar
  156. 156.
    Pérez-López P, Ternon E, González-García S et al (2014) Environmental solutions for the sustainable production of bioactive natural products from the marine sponge Crambe crambe. Sci Total Environ 475:71–82.  https://doi.org/10.1016/j.scitotenv.2013.12.068 CrossRefPubMedGoogle Scholar
  157. 157.
    Osinga R, Tramper J, Wijffels RH (1999b) Cultivation of marine sponges. Mar Biotechnol (NY) 1:509–532CrossRefGoogle Scholar
  158. 158.
    Hausmann R, Vitello MP, Leitermann F, Syldatk C (2006) Advances in the production of sponge biomass Aplysina aerophoba – a model sponge for ex situ sponge biomass production. J Biotechnol 124:117–127.  https://doi.org/10.1016/j.jbiotec.2006.03.033 CrossRefPubMedGoogle Scholar
  159. 159.
    Simpson TL (1984) Gamete, embryo, larval development. In: Simpson TL (ed) The cell biology of sponges. Springer, Berlin, pp 341–413CrossRefGoogle Scholar
  160. 160.
    Wilson HV (1907) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5:245–258.  https://doi.org/10.1002/jez.1400050204 CrossRefGoogle Scholar
  161. 161.
    Borojevic R (1966) Étude expérimentale de la différenciation des cellules de l’éponge au cours de son développement. Dev Biol 14:130–153.  https://doi.org/10.1016/0012-1606(66)90009-1 CrossRefPubMedGoogle Scholar
  162. 162.
    De Sutter D, Van de Vyver G (1979) Isolation and recognition properties of some definite sponge cell types. Dev Comp Immunol 3:389–397.  https://doi.org/10.1016/S0145-305X(79)80036-1 CrossRefPubMedGoogle Scholar
  163. 163.
    Pomponi SA (2006) Biology of the Porifera: cell culture. Can J Zool 84:167–174.  https://doi.org/10.1139/z05-188 CrossRefGoogle Scholar
  164. 164.
    Schippers KJ, Sipkema D, Osinga R et al (2012) Chapter six – cultivation of sponges, sponge cells and symbionts: achievements and future prospects. In: Mikel A, Becerro MJUMM, Xavier T (eds) Advances in marine biology. Academic, New York, pp 273–337Google Scholar
  165. 165.
    Pomponi SA, Willoughby R, Kaighn ME, Wright AE (1996) Development of techniques for in vitro production of bioactive natural products from marine sponges. In: Proceedings of the 1996 world congress of vitro biology, pp 231–237Google Scholar
  166. 166.
    Pomponi SA, Willoughby R, Kaighn ME, Wright AE (1997) Development of techniques for in vitro production of bioactive natural products from marine sponges. In: Maramorosch K, Mitsuhashi J (eds) Invertebrate cell culture: novel directions and biotechnology applications. Science Publishers, Enfield, NH, pp 231–237Google Scholar
  167. 167.
    Rinkevich B (2005) Marine invertebrate cell cultures: new millennium trends. Mar Biotechnol 7:429–439.  https://doi.org/10.1007/s10126-004-0108-y CrossRefPubMedGoogle Scholar
  168. 168.
    Cai X, Zhang Y (2014) Marine invertebrate cell culture: a decade of development. J Oceanogr 70:405–414.  https://doi.org/10.1007/s10872-014-0242-8 CrossRefGoogle Scholar
  169. 169.
    Willoughby R, Pomponi SA (2000) Quantitative assessment of marine sponge cells in vitro: development of improved growth medium. In Vitro Cell Dev Biol Anim 36:194–200CrossRefGoogle Scholar
  170. 170.
    Zhang X, Le Pennec G, Steffen R et al (2004) Application of a MTT assay for screening nutritional factors in growth media of primary sponge cell culture. Biotechnol Prog 20:151–155.  https://doi.org/10.1021/bp0341601 CrossRefPubMedGoogle Scholar
  171. 171.
    Custodio MR, Prokic I, Steffen R et al (1998) Primmorphs generated from dissociated cells of the sponge Suberites domuncula: a model system for studies of cell proliferation and cell death. Mech Ageing Dev 105:45–59.  https://doi.org/10.1016/S0047-6374(98)00078-5 CrossRefPubMedGoogle Scholar
  172. 172.
    Schippers KJ, Martens DE, Pomponi SA, Wijffels RH (2011) Cell cycle analysis of primary sponge cell cultures. In Vitro Cell Dev Biol Anim 47:302–311.  https://doi.org/10.1007/s11626-011-9391-x CrossRefPubMedPubMedCentralGoogle Scholar
  173. 173.
    Srivastava M, Simakov O, Chapman J et al (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726.  https://doi.org/10.1038/nature09201 CrossRefPubMedPubMedCentralGoogle Scholar
  174. 174.
    Schippers KJ (2013) Sponge cell culture. Dissertation, Wageningen UniversityGoogle Scholar
  175. 175.
    Pomponi SA, Jevitt A, Patel J, Diaz MC (2013) Sponge hybridomas: applications and implications. Integr Comp Biol 53:524–530CrossRefGoogle Scholar
  176. 176.
    Wijffels RH, Osinga R, Pomponi S, Tramper J (2001) Marine sponges as biocatalysts. In: Cabral JMS, Mota M, Tramper J (eds) Multiphase bioreactor design. Taylor & Francis, London, pp 477–493Google Scholar
  177. 177.
    Sipkema D, Schippers K, Maalcke WJ et al (2011) Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (gellius) sp. Appl Environ Microbiol 77:2130–2140.  https://doi.org/10.1128/AEM.01203-10 CrossRefPubMedPubMedCentralGoogle Scholar
  178. 178.
    Zhang H, Lee YK, Zhang W, Lee HK (2006) Culturable actinobacteria from the marine sponge Hymeniacidon perleve: isolation and phylogenetic diversity by 16S rRNA gene-RFLP analysis. Antonie Van Leeuwenhoek 90:159–169.  https://doi.org/10.1007/s10482-006-9070-1 CrossRefPubMedGoogle Scholar
  179. 179.
    Schwedt A, Seidel M, Dittmar T et al (2015) Substrate use of Pseudovibrio sp. growing in ultra-oligotrophic seawater. PLoS One 10:e0121675.  https://doi.org/10.1371/journal.pone.0121675 CrossRefPubMedPubMedCentralGoogle Scholar
  180. 180.
    Kurtböke DI (2005) Actinophages as indicators of actinomycete taxa in marine environments. Antonie Van Leeuwenhoek 87:19–28.  https://doi.org/10.1007/s10482-004-6535-y CrossRefPubMedGoogle Scholar
  181. 181.
    Rappe MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633CrossRefGoogle Scholar
  182. 182.
    Toledo G, Green W, Gonzalez R et al (2006) High throughput cultivation for isolation of novel marine microorganisms. Oceanography 19:120–125.  https://doi.org/10.5670/oceanog.2006.75 CrossRefGoogle Scholar
  183. 183.
    Steinert G, Whitfield S, Taylor MW et al (2014) Application of diffusion growth chambers for the cultivation of marine sponge-associated bacteria. Mar Biotechnol 16:594–603.  https://doi.org/10.1007/s10126-014-9575-y CrossRefPubMedGoogle Scholar
  184. 184.
    Reynolds D, Thomas T (2016) Evolution and function of eukaryotic-like proteins from sponge symbionts. Mol Ecol 25:5242–5253.  https://doi.org/10.1111/mec.13812 CrossRefPubMedGoogle Scholar
  185. 185.
    Janssen PH, Yates PS, Grinton BE et al (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68:2391–2396.  https://doi.org/10.1128/AEM.68.5.2391-2396.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  186. 186.
    Hoffmann F, Røy H, Bayer K et al (2008) Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba. Mar Biol 153:1257–1264.  https://doi.org/10.1007/s00227-008-0905-3 CrossRefPubMedPubMedCentralGoogle Scholar
  187. 187.
    Bruck WM, Bruck TB, Self WT et al (2010) Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida. ISME J 4:686–699CrossRefGoogle Scholar
  188. 188.
    Ueoka R, Uria AR, Reiter S et al (2015) Metabolic and evolutionary origin of actin-binding polyketides from diverse organisms. Nat Chem Biol 11:705–712.  https://doi.org/10.1038/nchembio.1870 CrossRefPubMedPubMedCentralGoogle Scholar
  189. 189.
    Lambalot RH, Gehring AM, Flugel RS et al (1996) A new enzyme superfamily – the phosphopantetheinyl transferases. Chem Biol 3:923–936.  https://doi.org/10.1016/S1074-5521(96)90181–7 CrossRefPubMedGoogle Scholar
  190. 190.
    Wenzel SC, Müller R (2005) Recent developments towards the heterologous expression of complex bacterial natural product biosynthetic pathways. Curr Opin Biotechnol 16:594–606.  https://doi.org/10.1016/j.copbio.2005.10.001 CrossRefPubMedGoogle Scholar
  191. 191.
    Borchert E, Jackson SA, O’Gara F, Dobson AD (2016) Diversity of natural product biosynthetic genes in the microbiome of the deep sea sponges Inflatella pellicula, Poecillastra compressa, and Stelletta normani. Front Microbiol 7:1027.  https://doi.org/10.3389/fmicb.2016.01027 CrossRefPubMedPubMedCentralGoogle Scholar
  192. 192.
    Kennedy J, Marchesi JR, Dobson ADW (2008) Marine metagenomics: strategies for the discovery of novel enzymes with biotechnological applications from marine environments. Microb Cell Factor 7:27.  https://doi.org/10.1186/1475-2859-7-27 CrossRefGoogle Scholar
  193. 193.
    Mineta K, Gojobori T (2016) Databases of the marine metagenomics. Gene 576:724–728.  https://doi.org/10.1016/j.gene.2015.10.035 CrossRefPubMedGoogle Scholar
  194. 194.
    Franzosa EA, Hsu T, Sirota-Madi A et al (2015) Sequencing and beyond: integrating molecular “omics” for microbial community profiling. Nat Rev Microbiol 13:360–372.  https://doi.org/10.1038/nrmicro3451 CrossRefPubMedPubMedCentralGoogle Scholar
  195. 195.
    Loman NJ, Pallen MJ (2015) Twenty years of bacterial genome sequencing. Nat Rev Microbiol 13:787–794.  https://doi.org/10.1038/nrmicro3565 CrossRefPubMedGoogle Scholar
  196. 196.
    Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77:1153–1161.  https://doi.org/10.1128/AEM.02345-10 CrossRefPubMedGoogle Scholar
  197. 197.
    Thomas T, Gilbert J, Meyer F (2012) Metagenomics – a guide from sampling to data analysis. Microb Inform Exp 2:3.  https://doi.org/10.1186/2042-5783-2-3 CrossRefPubMedPubMedCentralGoogle Scholar
  198. 198.
    Joyce AR, Palsson BO (2006) The model organism as a system: integrating “omics” data sets. Nat Rev Mol Cell Biol 7:198–210CrossRefGoogle Scholar
  199. 199.
    Webster NS, Thomas T (2016) Defining the sponge hologenome. MBio 7:1–14.  https://doi.org/10.1128/mBio.00135-16.Invited CrossRefGoogle Scholar
  200. 200.
    Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond Ser B Biol Sci 270:313CrossRefGoogle Scholar
  201. 201.
    Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522.  https://doi.org/10.1073/pnas.1000080107 CrossRefPubMedGoogle Scholar
  202. 202.
    Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA (2007) DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet 23:167–172.  https://doi.org/10.1016/j.tig.2007.02.001 CrossRefPubMedGoogle Scholar
  203. 203.
    Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109:6241–6246.  https://doi.org/10.1073/pnas.1117018109 CrossRefPubMedPubMedCentralGoogle Scholar
  204. 204.
    Vargas S, Schuster A, Sacher K et al (2012) Barcoding sponges: an overview based on comprehensive sampling. PLoS One 7:e39345.  https://doi.org/10.1371/journal.pone.0039345 CrossRefPubMedPubMedCentralGoogle Scholar
  205. 205.
    Hooper JNA, Soest RWM (2002) Systema porifera: a guide to the classification of sponges. Kluwer Academic/Plenum, New YorkCrossRefGoogle Scholar
  206. 206.
    Xavier JR, Rachello-Dolmen PG, Parra-Velandia F et al (2010) Molecular evidence of cryptic speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae). Mol Phylogenet Evol 56:13–20.  https://doi.org/10.1016/j.ympev.2010.03.030 CrossRefPubMedGoogle Scholar
  207. 207.
    Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. Annu Rev Mar Sci 3(3):471–508.  https://doi.org/10.1146/annurev-marine-120308-080950 CrossRefGoogle Scholar
  208. 208.
    Erpenbeck D, Ekins M, Enghuber N, et al (2015) Nothing in (sponge) biology makes sense – except when based on holotypes. J Mar Biol Assoc UK FirstView:1–7. doi: https://doi.org/10.1017/S0025315415000521 CrossRefGoogle Scholar
  209. 209.
    Wörheide G, Erpenbeck D, Menke C (2007) The Sponge Barcoding Project: aiding in the identification and description of poriferan taxa. Porifera Res Biodivers Innov Sustain:123–128Google Scholar
  210. 210.
    Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740CrossRefGoogle Scholar
  211. 211.
    Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedPubMedCentralGoogle Scholar
  212. 212.
    Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849CrossRefGoogle Scholar
  213. 213.
    Tringe SG, Hugenholtz P (2008) A renaissance for the pioneering 16S rRNA gene. Curr Opin Microbiol 11:442–446.  https://doi.org/10.1016/j.mib.2008.09.011 CrossRefPubMedGoogle Scholar
  214. 214.
    Althoff K, Schütt C, Steffen R et al (1998) Evidence for a symbiosis between bacteria of the genus Rhodobacter and the marine sponge Halichondria panicea : harbor also for putatively toxic bacteria? Mar Biol 130:529–536.  https://doi.org/10.1007/s002270050273 CrossRefGoogle Scholar
  215. 215.
    Webb VL, Maas EW (2002) Sequence analysis of 16S rRNA gene of cyanobacteria associated with the marine sponge Mycale (Carmia) hentscheli. FEMS Microbiol Lett 207:43–47CrossRefGoogle Scholar
  216. 216.
    Webster NS, Hill RT (2001) The culturable microbial community of the great barrier reef sponge Rhopaloeides odorabile is dominated by an Alphaproteobacterium. Mar Biol 138:843–851.  https://doi.org/10.1007/s002270000503 CrossRefGoogle Scholar
  217. 217.
    Friedrich AB, Merkert H, Fendert T et al (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134:461–470.  https://doi.org/10.1007/s002270050562 CrossRefGoogle Scholar
  218. 218.
    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.  https://doi.org/10.1073/pnas.93.13.6241 CrossRefPubMedPubMedCentralGoogle Scholar
  219. 219.
    Schmidt EW, Obraztsova AY, Davidson SK et al (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ-proteobacterium, “Candidatus Entotheonella palauensis”. Mar Biol 136:969–977.  https://doi.org/10.1007/s002270000273 CrossRefGoogle Scholar
  220. 220.
    Guardiola M, Uriz MJ, Taberlet P et al (2015) Deep-sea, deep-sequencing: metabarcoding extracellular DNA from sediments of marine canyons. PLoS One 10:e0139633.  https://doi.org/10.1371/journal.pone.0139633 CrossRefPubMedPubMedCentralGoogle Scholar
  221. 221.
    Zaiko A, Martinez JL, Schmidt-Petersen J et al (2015) Metabarcoding approach for the ballast water surveillance – an advantageous solution or an awkward challenge? Mar Pollut Bull 92:25–34.  https://doi.org/10.1016/j.marpolbul.2015.01.008 CrossRefPubMedGoogle Scholar
  222. 222.
    Chain FJJ, Brown EA, Macisaac HJ, Cristescu ME (2016) Metabarcoding reveals strong spatial structure and temporal turnover of zooplankton communities among marine and freshwater ports. Divers Distrib 22:493–504.  https://doi.org/10.1111/ddi.12427 CrossRefGoogle Scholar
  223. 223.
    Cowart DA, Pinheiro M, Mouchel O et al (2015) Metabarcoding is powerful yet still blind: a comparative analysis of morphological and molecular surveys of seagrass communities. PLoS One 10:1–26.  https://doi.org/10.1371/journal.pone.0117562 CrossRefGoogle Scholar
  224. 224.
    Leray M, Knowlton N (2015) DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proc Natl Acad Sci 112:2076–2081.  https://doi.org/10.1073/pnas.1424997112 CrossRefPubMedPubMedCentralGoogle Scholar
  225. 225.
    Stein L (2001) Genome annotation: from sequence to biology. Nat Rev Genet 2:493–503.  https://doi.org/10.1038/35080529 CrossRefPubMedGoogle Scholar
  226. 226.
    Wiens M, Grebenjuk VA, Schröder HC et al (2009) Identification and isolation of a retrotransposon from the freshwater sponge Lubomirskia baicalensis: implication in rapid evolution of endemic sponges. In: Biosilica in evolution, morphogenesis, and nanobiotechnology. Springer, Berlin, pp 207–234CrossRefGoogle Scholar
  227. 227.
    Perina D, Korolija M, Mikoč A et al (2012) Structural and functional characterization of ribosomal protein gene introns in sponges. PLoS One 7:1–9.  https://doi.org/10.1371/journal.pone.0042523 CrossRefGoogle Scholar
  228. 228.
    Radax R, Hoffmann F, Rapp HT et al (2012) Ammonia-oxidizing archaea as main drivers of nitrification in cold-water sponges. Environ Microbiol 14:909–923.  https://doi.org/10.1111/j.1462-2920.2011.02661.x CrossRefPubMedGoogle Scholar
  229. 229.
    Wilkinson CR, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527–529CrossRefGoogle Scholar
  230. 230.
    Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685.  https://doi.org/10.1128/MMBR.68.4.669-685.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  231. 231.
    Tringe SG, Rubin EM (2005) Metagenomics: DNA sequencing of environmental samples. Nat Rev Genet 6:805–814.  https://doi.org/10.1038/nrg1709 CrossRefPubMedGoogle Scholar
  232. 232.
    Tian RM, Wang Y, Bougouffa S et al (2014) Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur-oxidizing bacterium in sponge. Environ Microbiol 16:3548–3561.  https://doi.org/10.1111/1462-2920.12586 CrossRefPubMedGoogle Scholar
  233. 233.
    Burgsdorf I, Slaby BM, Handley KM et al (2015) Lifestyle evolution in cyanobacterial symbionts of sponges. MBio 6:1–14.  https://doi.org/10.1128/mBio.00391-15 CrossRefGoogle Scholar
  234. 234.
    Gao ZM, Wang Y, Tian RM et al (2014) Symbiotic adaptation drives genome streamlining of the cyanobacterial sponge symbiont ‘Candidatus Synechococcus spongiarum’. MBio 5:1–11.  https://doi.org/10.1128/mBio.00079-14 CrossRefGoogle Scholar
  235. 235.
    Gauthier M-EA, Watson JR, Degnan SM (2016) Draft genomes shed light on the dual bacterial symbiosis that dominates the microbiome of the coral reef sponge Amphimedon queenslandica. Front Mar Sci 3:1–18.  https://doi.org/10.3389/fmars.2016.00196 CrossRefGoogle Scholar
  236. 236.
    Ryu T, Seridi L, Moitinho-Silva L et al (2016) Hologenome analysis of two marine sponges with different microbiomes. BMC Genomics 17:158.  https://doi.org/10.1186/s12864-016-2501-0 CrossRefPubMedPubMedCentralGoogle Scholar
  237. 237.
    Trindade M, van Zyl LJ, Navarro-Fernandez J, Elrazak AA (2015) Targeted metagenomics as a tool to tap into marine natural product diversity for the discovery and production of drug candidates. Front Microbiol 6:1–14.  https://doi.org/10.3389/fmicb.2015.00890 CrossRefGoogle Scholar
  238. 238.
    Piel J, Hui D, Wen G et al (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc Natl Acad Sci U S A 101:16222–16227.  https://doi.org/10.1073/pnas.0405976101 CrossRefPubMedPubMedCentralGoogle Scholar
  239. 239.
    Fisch KM, Gurgui C, Heycke N et al (2009) Polyketide assembly lines of uncultivated sponge symbionts from structure-based gene targeting. Nat Chem Biol 5:494–501.  https://doi.org/10.1038/nchembio.176 CrossRefPubMedGoogle Scholar
  240. 240.
    Yung PY, Burke C, Lewis M et al (2011) Novel antibacterial proteins from the microbial communities associated with the sponge Cymbastela concentrica and the green alga Ulva australis. Appl Environ Microbiol 77:1512–1515.  https://doi.org/10.1128/AEM.02038-10 CrossRefPubMedGoogle Scholar
  241. 241.
    He R, Wang B, Wakimoto T et al (2013) Cyclodipeptides from metagenomic library of a Japanese marine sponge. J Braz Chem Soc 24:1926–1932.  https://doi.org/10.5935/0103-5053.20130240 CrossRefGoogle Scholar
  242. 242.
    Medema MH, Blin K, Cimermancic P et al (2011) AntiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39:339–346.  https://doi.org/10.1093/nar/gkr466 CrossRefGoogle Scholar
  243. 243.
    VanGuilder HD, Vrana KE, Freeman WM (2008) Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques 44:619–626.  https://doi.org/10.2144/000112776 CrossRefPubMedGoogle Scholar
  244. 244.
    Croucher NJ, Thomson NR (2010) Studying bacterial transcriptomes using RNA-seq. Curr Opin Microbiol 13:619–624.  https://doi.org/10.1016/j.mib.2010.09.009 CrossRefPubMedPubMedCentralGoogle Scholar
  245. 245.
    Engström PG, Steijger T, Sipos B et al (2013) Systematic evaluation of spliced alignment programs for RNA-seq data. Nat Methods 10:1185–1191.  https://doi.org/10.1038/nmeth.2722 CrossRefPubMedPubMedCentralGoogle Scholar
  246. 246.
    Steijger T, Abril JF, Engström PG et al (2013) Assessment of transcript reconstruction methods for RNA-seq. Nat Methods 10:1177–1184.  https://doi.org/10.1038/nmeth.2714 CrossRefPubMedGoogle Scholar
  247. 247.
    Aylward FO, Eppley JM, Smith JM et al (2015) Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proc Natl Acad Sci U S A 112:5443–5448.  https://doi.org/10.1073/pnas.1502883112 CrossRefPubMedPubMedCentralGoogle Scholar
  248. 248.
    Dyhrman S, Ammerman J, Van Mooy B (2007) Microbes and the marine phosphorus cycle. Oceanography 20:110–116.  https://doi.org/10.5670/oceanog.2007.54 CrossRefGoogle Scholar
  249. 249.
    Frias-Lopez J, Shi Y, Tyson G et al (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci 105:3805–3810CrossRefGoogle Scholar
  250. 250.
    Dunn CW, Leys SP, Haddock SHD (2015) The hidden biology of sponges and ctenophores. Trends Ecol Evol 30:282–291.  https://doi.org/10.1016/j.tree.2015.03.003 CrossRefPubMedGoogle Scholar
  251. 251.
    Jackson SA, Borchert E, O’Gara F, Dobson ADW (2015) Metagenomics for the discovery of novel biosurfactants of environmental interest from marine ecosystems. Curr Opin Biotechnol 33:176–182.  https://doi.org/10.1016/j.copbio.2015.03.004 CrossRefPubMedGoogle Scholar
  252. 252.
    Pawlik JR, McMurray SE, Erwin P, Zea S (2015) A review of evidence for food limitation of sponges on Caribbean reefs. Mar Ecol Prog Ser 519:265–283.  https://doi.org/10.3354/meps11093 CrossRefGoogle Scholar
  253. 253.
    Riesgo A, Farrar N, Windsor PJ et al (2014) The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Mol Biol Evol 31:1102–1120.  https://doi.org/10.1093/molbev/msu057 CrossRefPubMedGoogle Scholar
  254. 254.
    Guzman C, Conaco C (2016) Gene expression dynamics accompanying the sponge thermal stress response. PLoS One 11:1–15.  https://doi.org/10.1371/journal.pone.0165368 CrossRefGoogle Scholar
  255. 255.
    Leys SP (2015) Elements of a “nervous system” in sponges. J Exp Biol 218:581–591.  https://doi.org/10.1242/jeb.110817 CrossRefPubMedGoogle Scholar
  256. 256.
    Guzman C, Conaco C (2016) Comparative transcriptome analysis reveals insights into the streamlined genomes of haplosclerid demosponges. Sci Rep 6:18774.  https://doi.org/10.1038/srep18774 CrossRefPubMedPubMedCentralGoogle Scholar
  257. 257.
    Taylor MW, Hill RT, Hentschel U (2011) Meeting report: 1st international symposium on sponge microbiology. Mar Biotechnol 13:1057–1061.  https://doi.org/10.1007/s10126-011-9397-0 CrossRefPubMedGoogle Scholar
  258. 258.
    Richardson C, Hill M, Marks C et al (2012) Experimental manipulation of sponge/bacterial symbiont community composition with antibiotics: sponge cell aggregates as a unique tool to study animal/microorganism symbiosis. FEMS Microbiol Ecol 81:407–418.  https://doi.org/10.1111/j.1574-6941.2012.01365.x CrossRefPubMedGoogle Scholar
  259. 259.
    Riesgo A, Peterson K, Richardson C et al (2014) Transcriptomic analysis of differential host gene expression upon uptake of symbionts: a case study with Symbiodinium and the major bioeroding sponge Cliona varians. BMC Genomics 15:376.  https://doi.org/10.1186/1471-2164-15-376 CrossRefPubMedPubMedCentralGoogle Scholar
  260. 260.
    Díez-Vives C, Moitinho-Silva L, Nielsen S et al (2016) Expression of eukaryotic-like protein in the microbiome of sponges. Mol Ecol.  https://doi.org/10.1111/mec.14003
  261. 261.
    Anderson NL, Anderson NG (1998) Proteome and proteomics: new technologies, new concepts, and new words. Electrophoresis 19:1853–1861.  https://doi.org/10.1002/elps.1150191103 CrossRefPubMedGoogle Scholar
  262. 262.
    Blackstock WP, Weir MP (1999) Proteomics: quantitative and physical mapping of cellular proteins. Trends Biotechnol 17:121–127.  https://doi.org/10.1016/S0167-7799(98)01245-1 CrossRefPubMedGoogle Scholar
  263. 263.
    James P (1997) Protein identification in the post-genome era: the rapid rise of proteomics. Q Rev Biophys 30:279–331.  https://doi.org/10.1017/S0033583597003399 CrossRefPubMedGoogle Scholar
  264. 264.
    Christie-Oleza JA, Fernandez B, Nogales B et al (2012) Proteomic insights into the lifestyle of an environmentally relevant marine bacterium. ISME J 6:124–135.  https://doi.org/10.1038/ismej.2011.86 CrossRefPubMedGoogle Scholar
  265. 265.
    Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5:3–21.  https://doi.org/10.1007/s11306-008-0152-0 CrossRefGoogle Scholar
  266. 266.
    Oliver S (1998) Systematic functional analysis of the yeast genome. Trends Biotechnol 16:373–378.  https://doi.org/10.1016/S0167-7799(98)01214-1 CrossRefPubMedGoogle Scholar
  267. 267.
    Ivanišević J, Thomas OP, Lejeusne C et al (2011) Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 7:289–304.  https://doi.org/10.1007/s11306-010-0239-2 CrossRefGoogle Scholar
  268. 268.
    Viegelmann C, Margassery LM, Kennedy J et al (2014) Metabolomic profiling and genomic study of a marine sponge-associated Streptomyces sp. Mar Drugs 12:3323–3351.  https://doi.org/10.3390/md12063323 CrossRefPubMedPubMedCentralGoogle Scholar
  269. 269.
    Nicholson JK, Lindon JC (2008) Systems biology: metabonomics. Nature 455:1054–1056.  https://doi.org/10.1038/4551054a CrossRefPubMedGoogle Scholar
  270. 270.
    Holmes E, Loo RL, Stamler J et al (2008) Human metabolic phenotype diversity and its association with diet and blood pressure. Nature 453:396–400CrossRefGoogle Scholar
  271. 271.
    Holmes E, Wilson ID, Nicholson JK (2008) Metabolic phenotyping in health and disease. Cell 134:714–717.  https://doi.org/10.1016/j.cell.2008.08.026 CrossRefPubMedGoogle Scholar
  272. 272.
    Marchesi JR, Holmes E, Khan F et al (2007) Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res 6:546–551.  https://doi.org/10.1021/pr060470d CrossRefPubMedGoogle Scholar
  273. 273.
    Nicholson JK, Lindon JC, Holmes E (1999) “Metabonomics”: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29:1181–1189.  https://doi.org/10.1080/004982599238047 CrossRefPubMedGoogle Scholar
  274. 274.
    Midelfart A (2009) Metabonomics – a new approach in ophthalmology. Acta Ophthalmol 87:697–703.  https://doi.org/10.1111/j.1755-3768.2009.01516.x CrossRefPubMedGoogle Scholar
  275. 275.
    Zhao YY, Cheng XL, Wei F et al (2012) Application of faecal metabonomics on an experimental model of tubulointerstitial fibrosis by ultra performance liquid chromatography/high-sensitivity mass spectrometry with MSE data collection technique. Biomarkers 17:721–729.  https://doi.org/10.3109/1354750x.2012.724450 CrossRefPubMedGoogle Scholar
  276. 276.
    Boroujerdi AFB, Vizcaino MI, Meyers A et al (2009) NMR-based microbial metabolomics and the temperature-dependent coral pathogen Vibrio coralliilyticus. Environ Sci Technol 43:7658–7664.  https://doi.org/10.1021/es901675w CrossRefPubMedGoogle Scholar
  277. 277.
    Ramirez-Llodra E, Brandt A, Danovaro R et al (2010) Deep, diverse and definitely different: unique attributes of the world’s largest ecosystem. Biogeosciences 7:2851–2899.  https://doi.org/10.5194/bg-7-2851-2010 CrossRefGoogle Scholar
  278. 278.
    Jorgensen BB, Boetius A (2007) Feast and famine – microbial life in the deep-sea bed. Nat Rev Microbiol 5:770–781CrossRefGoogle Scholar
  279. 279.
    Zierenberg RA, Adams MWW, Arp AJ (2000) Life in extreme environments: hydrothermal vents. Proc Natl Acad Sci 97:12961–12962.  https://doi.org/10.1073/pnas.210395997 CrossRefPubMedPubMedCentralGoogle Scholar
  280. 280.
    Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353.  https://doi.org/10.1016/j.ecss.2008.05.002 CrossRefGoogle Scholar
  281. 281.
    Jackson SA, Flemer B, McCann A et al (2014) Archaea appear to dominate the microbiome of Inflatella pellicula deep sea sponges. PLoS One 8:e84438.  https://doi.org/10.1371/journal.pone.0084438 CrossRefGoogle Scholar
  282. 282.
    Kennedy J, Flemer B, Jackson SA et al (2014) Evidence of a putative deep sea specific microbiome in marine sponges. PLoS One 9:e91092.  https://doi.org/10.1371/journal.pone.0091092 CrossRefPubMedPubMedCentralGoogle Scholar
  283. 283.
    Sipkema D (2016) Marine biotechnology: diving deeper for drugs. Microb Biotechnol.  https://doi.org/10.1111/1751-7915.12410
  284. 284.
    OSPAR Commission (2010) Background document for deep-sea sponge aggregations. OSPAR Biodivers Ecosyst Ser 47Google Scholar
  285. 285.
    Lundsten L, Reiswig HM, Austin WC (2014) Four new species of Cladorhizidae (Porifera, Demospongiae, Poecilosclerida) from the Northeast Pacific. Zootaxa 3786:101–123.  https://doi.org/10.11646/zootaxa.3786.2.1 CrossRefPubMedGoogle Scholar
  286. 286.
    Vacelet J, Boury-Esnault N, Fiala-Medioni A, Fisher CR (1995) A methanotrophic carnivorous sponge. Nature 377:296–296CrossRefGoogle Scholar
  287. 287.
    Ritzau M, Keller M, Wessels P et al (1993) New cyclic polysulfides from hyperthermophilic archaea of the genus Thermococcus. Liebigs Ann Chem 8:871–876CrossRefGoogle Scholar
  288. 288.
    Huber H, Stetter KO (1998) Hyperthermophiles and their possible potential in biotechnology. J Biotechnol 64:39–52.  https://doi.org/10.1016/S0168-1656(98)00102-3 CrossRefGoogle Scholar
  289. 289.
    Dridi B, Fardeau ML, Ollivier B et al (2011) The antimicrobial resistance pattern of cultured human methanogens reflects the unique phylogenetic position of archaea. J Antimicrob Chemother 66:2038–2044.  https://doi.org/10.1093/jac/dkr251 CrossRefPubMedGoogle Scholar
  290. 290.
    Margot H, Acebal C, Toril E et al (2002) Consistent association of crenarchaeal Archaea with sponges of the genus Axinella. Mar Biol 140:739–745.  https://doi.org/10.1007/s00227-001-0740-2 CrossRefGoogle Scholar
  291. 291.
    Erwin PM, Pineda MC, Webster N et al (2014) Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians. ISME J 8:575–588.  https://doi.org/10.1038/ismej.2013.188 CrossRefPubMedGoogle Scholar
  292. 292.
    Siboni N, Ben-Dov E, Sivan A, Kushmaro A (2008) Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10:2979–2990.  https://doi.org/10.1111/j.1462-2920.2008.01718.x CrossRefPubMedGoogle Scholar
  293. 293.
    Steinert G, Taylor MW, Schupp PJ (2015) Diversity of Actinobacteria associated with the marine ascidian Eudistoma toealensis. Mar Biotechnol 17:377–385.  https://doi.org/10.1007/s10126-015-9622-3 CrossRefPubMedGoogle Scholar
  294. 294.
    Simon HM, Jahn CE, Bergerud LT et al (2005) Cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots. Appl Environ Microbiol 71:4751–4760.  https://doi.org/10.1128/AEM.71.8.4751 CrossRefPubMedPubMedCentralGoogle Scholar
  295. 295.
    Dobson ADW, Jackson SA, Kennedy J et al (2015) Marine sponges – molecular biology and biotechnology. In: Kim S-K (ed) Springer handbook of marine biotechnology. Springer, Berlin, pp 219–254CrossRefGoogle Scholar
  296. 296.
    Höller U, Wright AD, Matthee GF et al (2000) Fungi from marine sponges: diversity, biological activity and secondary metabolites. Mycol Res 104:1354–1365.  https://doi.org/10.1017/S0953756200003117 CrossRefGoogle Scholar
  297. 297.
    Pivkin MV, Aleshko SA, Krasokhin VB, Khudyakova YV (2006) Fungal assemblages associated with sponges of the southern coast of Sakhalin Island. Russ J Mar Biol 32:207–213.  https://doi.org/10.1134/S1063074006040018 CrossRefGoogle Scholar
  298. 298.
    Suttle CA (2005) Viruses in the sea. Nature 437:356–361CrossRefGoogle Scholar
  299. 299.
    Mojica KDA, Brussaard CPD (2014) Factors affecting virus dynamics and microbial host–virus interactions in marine environments. FEMS Microbiol Ecol 89:495–515.  https://doi.org/10.1111/1574-6941.12343 CrossRefPubMedGoogle Scholar
  300. 300.
    Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5:801–812.  https://doi.org/10.1038/nrmicro1750 CrossRefPubMedGoogle Scholar
  301. 301.
    Claverie J-M, Grzela R, Lartigue A et al (2009) Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J Invertebr Pathol 101:172–180.  https://doi.org/10.1016/j.jip.2009.03.011 CrossRefPubMedGoogle Scholar
  302. 302.
    Laffy PW, Wood-Charlson EM, Turaev D et al (2016) HoloVir: a workflow for investigating the diversity and function of viruses in invertebrate holobionts. Front Microbiol 7:822.  https://doi.org/10.3389/fmicb.2016.00822 CrossRefPubMedPubMedCentralGoogle Scholar
  303. 303.
    Roux S, Tournayre J, Mahul A et al (2014) Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinformatics 15:76.  https://doi.org/10.1186/1471-2105-15-76 CrossRefPubMedPubMedCentralGoogle Scholar
  304. 304.
    Wommack KE, Bhavsar J, Polson SW et al (2012) VIROME: a standard operating procedure for analysis of viral metagenome sequences. Stand Genomic Sci 6:427–439.  https://doi.org/10.4056/sigs.2945050 CrossRefPubMedPubMedCentralGoogle Scholar
  305. 305.
    Lorenzi HA, Hoover J, Inman J et al (2011) TheViral MetaGenome Annotation Pipeline (VMGAP): an automated tool for the functional annotation of viral metagenomic shotgun sequencing data. Stand Genomic Sci 4:418–429.  https://doi.org/10.4056/sigs.1694706 CrossRefPubMedPubMedCentralGoogle Scholar
  306. 306.
    Maciejewska B, Roszniowski B, Espaillat A et al (2017) Klebsiella phages representing a novel clade of viruses with an unknown DNA modification and biotechnologically interesting enzymes. Appl Microbiol Biotechnol 101:673–684.  https://doi.org/10.1007/s00253-016-7928-3 CrossRefPubMedGoogle Scholar
  307. 307.
    Freeman MF, Helf MJ, Bhushan A et al (2016) Seven enzymes create extraordinary molecular complexity in an uncultivated bacterium. Nat Chem.  https://doi.org/10.1038/nchem.2666

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Georg Steinert
    • 1
  • Carla Huete Stauffer
    • 2
  • Nele Aas-Valleriani
    • 3
  • Erik Borchert
    • 4
  • Agneya Bhushan
    • 5
  • Alexandra Campbell
    • 6
  • Maryam Chaib De Mares
    • 7
  • Margarida Costa
    • 8
  • Johanna Gutleben
    • 1
  • Stephen Knobloch
    • 9
  • Robert Gregory Lee
    • 10
  • Stephanie Munroe
    • 11
    • 12
  • Deepak Naik
    • 13
  • Eike Edzard Peters
    • 5
  • Ellen Stokes
    • 10
  • Wanlin Wang
    • 14
  • Eydís Einarsdóttir
    • 15
  • Detmer Sipkema
    • 1
  1. 1.Laboratory of MicrobiologyWageningen UniversityWageningenThe Netherlands
  2. 2.Marine Ecology DepartmentCentre d’Estudis Avançats de Blanes (CEAB), Consejo Superior de Investigaciones Científicas (CSIC)BlanesSpain
  3. 3.Tallinn University of TechnologyTallinnEstonia
  4. 4.School of Microbiology, University College Cork, National University of IrelandCorkIreland
  5. 5.Institute of Microbiology, Eidgenössische Technische Hochschule ZürichZürichSwitzerland
  6. 6.School of Biosciences, Cardiff UniversityCardiffUK
  7. 7.Microbial Ecology Group, Genomic Research in Ecology and Evolution in Nature (GREEN)Groningen Institute for Evolutionary Life Sciences (GELIFES), University of GroningenGroningenThe Netherlands
  8. 8.Faculty of Pharmaceutical SciencesUniversity of IcelandReykjavíkIceland
  9. 9.Department of Research and InnovationMatis ohf.ReykjavikIceland
  10. 10.Birmingham Law School, University of BirminghamBirminghamUK
  11. 11.Division of Bioprocess EngineeringWageningen UniversityWageningenThe Netherlands
  12. 12.Harbor Branch Oceanographic Institute, Florida Atlantic UniversityBoca RatonUSA
  13. 13.Department of Microbial Ecology and Diversity ResearchLeibniz Institute DSMZ – German Collection of Microorganisms and Cell CulturesBraunschweigGermany
  14. 14.Sustainable Place Research Institute, Cardiff UniversityCardiffUK
  15. 15.Pharma Mar, S.A.MadridSpain

Personalised recommendations