Skip to main content

Advertisement

SpringerLink
Log in

Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In this study, we used a 16S rRNA gene barcoded pyrosequencing approach to sample bacterial communities from six biotopes, namely, seawater, sediment and four sponge species (Stylissa carteri, Stylissa massa, Xestospongia testudinaria and Hyrtios erectus) inhabiting coral reefs of the Spermonde Archipelago, South Sulawesi, Indonesia. Samples were collected along a pronounced onshore to offshore environmental gradient. Our goals were to (1) compare higher taxon abundance among biotopes, (2) test to what extent variation in bacterial composition can be explained by the biotope versus environment, (3) identify dominant (>300 sequences) bacterial operational taxonomic units (OTUs) and their closest known relatives and (4) assign putative functions to the sponge bacterial communities using a recently developed predictive metagenomic approach. We observed marked differences in bacterial composition and the relative abundance of the most abundant phyla, classes and orders among sponge species, seawater and sediment. Although all biotopes housed compositionally distinct bacterial communities, there were three prominent clusters. These included (1) both Stylissa species and seawater, (2) X. testudinaria and H. erectus and (3) sediment. Bacterial communities sampled from the same biotope, but different environments (based on proximity to the coast) were much more similar than bacterial communities from different biotopes in the same environment. The biotope thus appears to be a much more important structuring force than the surrounding environment. There were concomitant differences in the predicted counts of KEGG orthologs (KOs) suggesting that bacterial communities housed in different sponge species, sediment and seawater perform distinct functions. In particular, the bacterial communities of both Stylissa species were predicted to be enriched for KOs related to chemotaxis, nitrification and denitrification whereas bacterial communities in X. testudinaria and H. erectus were predicted to be enriched for KOs related to the toxin–antitoxin (TA) system, nutrient starvation and heavy metal export.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, Srivastava DS (2004) Extinction and ecosystem function in the marine benthos. Science 306:1177–1180

    Article  CAS  PubMed  Google Scholar 

  2. Carpenter KE, Arbar M, Aeby G, Aronson RB et al (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    Article  CAS  PubMed  Google Scholar 

  3. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  CAS  PubMed  Google Scholar 

  4. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958

    Article  CAS  PubMed  Google Scholar 

  5. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:e711

    Article  PubMed Central  PubMed  Google Scholar 

  6. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci U S A 109:17995–17999

    Article  PubMed Central  PubMed  Google Scholar 

  7. Done TJ, DeVantier LM, Turak E, Fisk DA, Wakeford M, van Woesik R (2010) Coral growth on three reefs: development of recovery benchmarks using a space for time approach. Coral Reefs 29:815–833

    Article  Google Scholar 

  8. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642

    Article  PubMed  Google Scholar 

  9. Garren M, Azam F (2012) New directions in coral reef microbial ecology. Environ Microbiol 14:833–844. doi:10.1111/j.1462-2920.2011.02597.x

    Article  CAS  PubMed  Google Scholar 

  10. Diaz MC, Rutzler K (2001) Sponges: an essential component of Caribbean coral reefs. B Mar Sci 69:535–546

    Google Scholar 

  11. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J, Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68:4431–4440

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654

    Article  CAS  PubMed  Google Scholar 

  13. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177

    Article  CAS  PubMed  Google Scholar 

  14. Kamke J, Taylor M, Schmitt S (2010) Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME J 4:498–508

    Article  CAS  PubMed  Google Scholar 

  15. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol R 71:295–347

    Article  CAS  Google Scholar 

  16. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, Thomas T (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci U S A 109:E1878–E1887

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A, Qian PY (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5:650–664. doi:10.1038/ismej.2010.165

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Moitinho-Silva L, Seridi L, Ryu T, Voolstra CR, Ravasi T, Hentschel U (2014) Revealing microbial functional activities in the Red Sea sponge Stylissa carteri by metatranscriptomics. Environ Microbiol. doi:10.1111/1462-2920.12533

    PubMed  Google Scholar 

  19. Radax R, Rattei T, Lanzen A, Bayer C, Rapp HT, Urich T, Schleper C (2012) Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. Environ Microbiol 14:1308–1324

    Article  CAS  PubMed  Google Scholar 

  20. Sanders JG, Beinart RA, Stewart FJ, Delong EF, Girguis PR (2013) Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. ISME J 7:1556–1567

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. McLeod E, Timmermann A, Salm R et al (2010) Warming seas in the Coral Triangle: coral reef vulnerability and management implications. Coast Manag 38:518–539

    Article  Google Scholar 

  22. Bell JJ, Davy SK, Jones T , Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Glob Chang Biol 19:2613–2624

  23. McMurray SE, Henkel TP, Pawlik JR (2010) Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology 91:560–570

    Article  PubMed  Google Scholar 

  24. Montalvo NF, Hill RT (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Environ Microbiol 77:7207–7216

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. doi:10.1038/nbt.2676

    Article  CAS  PubMed  Google Scholar 

  26. de Voogd NJ, Cleary DFR, Hoeksema B, Noor A, van Soest R (2006) Sponge beta diversity in the Spermonde Archipelago, SW Sulawesi, Indonesia. Mar Ecol-Prog Ser 309:131–142

    Article  Google Scholar 

  27. Renema W (2010) Is increased calcarinid (foraminifera) abundance indicating a larger role for macro-algae in Indonesian Plio-Pleistocene coral reefs? Coral Reefs 29:165–173

    Article  Google Scholar 

  28. Cleary DFR, Becking LE, Voogd NJ, Pires ACC, Polónia ARM, Egas C, Gomes NCM (2013) Habitat-and host-related variation in sponge bacterial symbiont communities in Indonesian waters. FEMS Microbiol Ecol 85:465–482

    Article  CAS  PubMed  Google Scholar 

  29. Cleary DFR, Renema W (2007) Relating species traits of foraminifera to environmental parameters in the Spermonde Archipelago, Indonesia. Mar Ecol-Prog Ser 334:73–82

    Article  Google Scholar 

  30. de Voogd NJ, Cleary DFR (2007) Relating species traits to environmental variables in Indonesian coral reef sponge assemblages. Mar Freshw Res 58:240–249

    Article  Google Scholar 

  31. Renema W, Troelstra SR (2001) Larger foraminifera distribution on a mesotrophic carbonate shelf in SW Sulawesi (Indonesia). Palaeogeogr, Palaeoclim, Palaeoecol 175:125–146

    Article  Google Scholar 

  32. de Klerk LG (1983) Zeespiegels, riffen en kustvlakten in Zuidwest Sulawesi, Indonesië; een morphogenetisch-bodemkundige studie. Utrecht, the Netherlands, Pp. 174

  33. Hoeksema BW, Moka W (1989) Species assemblages and phenotypes of mushroom corals (Fungiidae) related to coral reef habitats in the Flores Sea. Neth J Sea Res 23:149–160

    Article  Google Scholar 

  34. Erftemeijer PLA (1994) Differences in nutrient concentrations and resources between seagrass communities on carbonate and terrigenous sediments in South Sulawesi, Indonesia. Bull Mar Sci 54:403–419

    Google Scholar 

  35. Capone DG, Dunham SE, Horrigan SG, Duguay LE (1992) Microbial nitrogen transformations in unconsolidated coral reef sediments. Mar Ecol-Prog Ser 80:75–88

    Article  CAS  Google Scholar 

  36. Polónia ARM, Cleary DRF, Duarte LN, de Voogd NJ, Gomes NCM (2013) Composition of Archaea in seawater, sediment and sponges in the Kepulauan Seribu reef system, Indonesia. Microb Ecol 67:553–567

    Article  Google Scholar 

  37. Bowen JL, Morrison HG, Hobbie JE, Sogin ML (2012) Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. ISME J 6:2014–2023

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci U S A 103:12115–12120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Cleary DFR, Becking LE, de Voogd NJ, Renema W, de Beer M, van Soest RWM, Hoeksema BW (2005) Variation in the diversity and composition of benthic taxa as a function of distance offshore, depth and exposure in the Spermonde Archipelago, Indonesia. Estuar Coast Shelf Sci 65:557–570

    Article  Google Scholar 

  40. Previsic A, Walton C, Kucinic M, Mitrikeski PT, Kerovec M (2009) Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol Ecol 18:634–647

    Article  CAS  PubMed  Google Scholar 

  41. Costa R, Keller-Costa T, Gomes NCM, da Rocha, Ulisses N, van Overbeek L, van Elsas JD (2013) Evidence for selective bacterial community structuring in the freshwater sponge Ephydatia fluviatilis. Microb Ecol 65:232–244

    Article  PubMed  Google Scholar 

  42. Urakawa H, Martens-Habbena W, Stahl DA (2010) High abundance of ammonia-oxidizing Archaea in coastal waters, determined using a modified DNA extraction method. App Environ Microb 76:2129–2135

    Article  CAS  Google Scholar 

  43. Gomes NCM, Heuer H, Schönfeld J, Costa RS, Mendonça-Hagler LCS et al (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180. doi:10.1023/A:1010350406708

    Article  CAS  Google Scholar 

  44. Wang Y, Qian P (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4:e7401

    Article  PubMed Central  PubMed  Google Scholar 

  45. Pires ACC, Cleary DFR, Almeida A, Cunha Â, Dealtry S, Mendonça-Hagler LCS, Smalla K, Gomes NCM (2012) Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. App Environ Microb 78:5520–5528

    Article  CAS  Google Scholar 

  46. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughp community sequencing data. Nat Methods 7:335–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  48. Edgar R, Haas B, Clemente J, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

  50. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available from http://www.R-project.org/

  51. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson G, Solymos P, Stevens M, Wagner H (2009) Vegan: Community ecology package. R package version 1.15–2. URL:http://CRAN.R-project.org/package=vegan

  52. Cleary DFR (2003) An examination of scale of assessment, logging and ENSO-induced fires on butterfly diversity in Borneo. Oecologia 135:313–321

    Article  PubMed  Google Scholar 

  53. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  54. de Voogd NJ, Cleary DRF, Polónia ARM, Gomes NCM (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand island reef complex, West-Java, Indonesia. FEMS Microbiol Ecol. 91(4):1:12. pii: fiv019. doi:10.1093/femsec/fiv019

  55. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38:105–113

    Article  CAS  Google Scholar 

  56. Reveillaud J, Maignien L, Murat Eren A, Huber JA, Apprill A, Sogin ML, Vanreusel A (2014) Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8:1198–1209. doi:10.1038/ismej.2013.227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Hawlena H, Rynkiewicz E, Toh E, Alfred A, Durden LA, Hastriter MW, Nelson DE, Rong R, Munro D, Dong Q, Fuqua C, Clay K (2013) The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J 7:221–223. doi:10.1038/ismej.2012.71

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Dinasquet J, Kragh T, Schrøter ML, Søndergaard M, Riemann L (2013) Functional and compositional succession of bacterioplankton in response to a gradient in bioavailable dissolved organic carbon. Environ Microbiol 15:2616–2628. doi:10.1111/1462-2920.12178

    Article  CAS  PubMed  Google Scholar 

  59. Ngugi DK, Antunes A, Brune A, Stingl U (2012) Biogeography of pelagic bacterioplankton across an antagonistic temperature-salinity gradient in the Red Sea. Mol Ecol 21:388–405. doi:10.1111/j.1365-294X.2011.05378.x

    Article  CAS  PubMed  Google Scholar 

  60. Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. App Environ Microb 74:7694–7708

    Article  CAS  Google Scholar 

  61. Giles EC, Kamke J, Moitinho-Silva L, Taylor MW, Hentschel U, Ravasi T, Schmitt S (2013) Bacterial community profiles in low microbial abundance sponges. FEMS Microbiol Ecol 83:232–241

    Article  CAS  PubMed  Google Scholar 

  62. Webster NS, Luter HM, Soo RM, Botte ES, Simister RL, Abdo D, Whalan S (2012) Same, same but different: symbiotic bacterial associations in GBR sponges. Front Microbiol 3:444. doi:10.3389/fmicb.2012.00444

    PubMed Central  CAS  PubMed  Google Scholar 

  63. Han M, Liu F, Zhang F, Li Z, Lin H (2012) Bacterial and archaeal symbionts in the South China Sea sponge Phakellia fusca: community structure, relative abundance, and ammonia-oxidizing populations. Mar Biotechnol 14:701–713

    Article  CAS  PubMed  Google Scholar 

  64. Polónia ARM, Cleary DRF, Freitas R, de Voogd NJ, Gomes NCM (2015) The putative functional ecology and distribution of archaeal communities in sponges, sediment and seawater in a coral reef environment. Mol Ecol 24:409–423. doi:10.1111/mec.13024

    Article  PubMed  Google Scholar 

  65. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster N, Hentschel U, Taylor MW (2011) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576

    Article  PubMed Central  PubMed  Google Scholar 

  67. Erpenbeck D, Sutcliffe P, Cook SC, Dietzel A, Maldonado M, van Soest RWM, Hooper JNA, Wörheide G (2012) Horny sponges and their affairs: on the phylogenetic relationships of keratose sponges. Mol Phylogenet Evol 63:809–816. doi:10.1016/j.ympev.2012.02.024

    Article  PubMed  Google Scholar 

  68. Easson CG, Thacker RW (2014) Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front Microbiol 5:532. doi:10.3389/fmicb.2014.00532

    PubMed Central  PubMed  Google Scholar 

  69. Desqueyroux-Faúndez R, Valentine C (2002) Family Petrosiidae Van Soest, 1980. In: Hooper JNA, Van Soest RWM (eds) Systema Porifera. A guide to the classification of sponges. 1 (Kluwer Academic/ Plenum Publishers, New York, pp 906–917

    Google Scholar 

  70. Van Soest RWM, Erpenbeck D, Alvarez B (2002) Family Dictyonellidae Van Soest, Diaz & Pomponi, 1990. In: Hooper JNA, Van Soest RWM, Willenz P (eds) Systema Porifera. Springer, US, pp 773–786

    Chapter  Google Scholar 

  71. Kennedy J, Flemer B, Jackson SA, Morrissey JP, O’Gara F, Dobson ADW (2014) Evidence of a putative deep sea specific microbiome in marine sponges. PLoS One 9:e91092. doi:10.1371/journal.pone.0091092

    Article  PubMed Central  PubMed  Google Scholar 

  72. Moitinho-Silva L, Bayer K, Cannistraci CV, Giles EC, Ryu T, Seridi L, Ravasi T, Hentschel U (2014) Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea. Mol Ecol 23:1348–1363

    Article  CAS  PubMed  Google Scholar 

  73. Gloeckner V, Hentschel U, Ereskovsky AV, Schmitt S (2013) Unique and species-specific microbial communities in Oscarella lobularis and other Mediterranean Oscarella species (Porifera: Homoscleromorpha). Mar Biol 160:781–791. doi:10.1007/s00227-012-2133-0

    Article  CAS  Google Scholar 

  74. Thacker RW, Freeman CJ (2012) Sponge-microbe symbioses: recent advances and new directions. Advances in Sponge Science: Physiology, Chemical and Microbial Diversity, Biotechnology. Becerro MA, Uriz MJ, Maldonado M, Turon X. San Diego, Elsevier Academic Press Inc. 62: 57–111

  75. Weisz JB, Lindquist N, Martens CS (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities. Oecologia 155:367–376. doi:10.1007/s00442-007-0910-0

    Article  PubMed  Google Scholar 

  76. Ribes M, Jimenez E, Yahel G, Lopez-Sendino P, Diez B, Massana R, Sharp JH, Coma R (2012) Functional convergence of microbes associated with temperate marine sponges. Environ Microbiol 14:1224–1239

    Article  CAS  PubMed  Google Scholar 

  77. Levipan HA, Molina V (2014) Fernandez C (2014) Nitrospina-like bacteria are the main drivers of nitrite oxidation in the seasonal upwelling area of the Eastern South Pacific (Central Chile ~36°S). Environ Microbiol Rep. doi:10.1111/1758-2229.12158

    PubMed  Google Scholar 

  78. Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280:1448–1456

    Article  CAS  PubMed  Google Scholar 

  79. Laub MT, Goulian M (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41:121–145

    Article  CAS  PubMed  Google Scholar 

  80. Cooper TF, Heinemann JA (2000) Postsegregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids. Proc Natl Acad Sci U S A 97:12643–12648. doi:10.1073/pnas.220077897

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  81. Schureck MA, Maehigashi T, Miles SJ, Marquez J, Cho SE, Erdman R, Dunham CM (2014) Structure of the Proteus vulgaris HigB-(HigA)2-HigB toxin-antitoxin complex. J Biol Chem 289:1060–1070. doi:10.1074/jbc.M113.512095

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  82. Wen Y, Behiels E, Devreese B (2014) Toxin–Antitoxin systems: their role in persistence, biofilm formation, and pathogenicity. Pathog Dis 70:240–249. doi:10.1111/2049-632X.12145

    Article  CAS  PubMed  Google Scholar 

  83. Pandey DP, Gerdes K (2005) Toxin–antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 33:966–976

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  84. Li D, Xu Y, Shao CL, Yang RY, Zheng CJ, Chen YY, Fu XM, Qian PY, She ZG, de Voogd NJ, Wang CY (2012) Antibacterial bisabolane-type sesquiterpenoids from the sponge-derived fungus Aspergillus sp. Mar Drugs 10:234–241. doi:10.3390/md10010234

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  85. Thakur NL, Hentschel U, Krasko A, Pabel CT, Anil AC, Müller WEG (2003) Antibacterial activity of the sponge Suberites domuncula and its primmorphs: potential basis for epibacterial chemical defense. Aquat Microb Ecol 31:77–83

    Article  Google Scholar 

  86. Bell JJ, Smith D, Hannan D, Haris A, Jompa J, Thomas L (2014) Resilience to disturbance despite limited dispersal and self-recruitment in tropical barrel sponges: implications for conservation and management. PLoS One 9:e91635. doi:10.1371/journal.pone.0091635

    Article  PubMed Central  PubMed  Google Scholar 

  87. de Voogd NJ, Cleary DFR (2009) Variation in sponge composition among Singapore reefs. Raffles B Zool Supp 22:59–67

    Google Scholar 

  88. Swierts T, Peijnenburg KTCA, Cleary DFR, Hörnlein C, Setiawan E, Wörheide G, Erpenbeck D, de Voogd NJ (2013) Lock, stock and two different barrels: morphological and genetic variation of the Indo-Pacific sponge Xestospongia testudinaria around Lembeh Island, Indonesia. PLoS One 8:e74396. doi:10.1371/journal.pone.0074396

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  89. Carstens J, Heinrich MR, Steglich W (2013) Studies on the synthesis and biosynthesis of the fungal alkaloid necatorone. Tetrahedron Lett 54:5445–5447

    Article  CAS  Google Scholar 

  90. Kibet JK, Khachatryan L, Dellinger B (2013) Molecular products from the pyrolysis and oxidative pyrolysis of tyrosine. Chemosphere 91:1026–1034

    Article  CAS  PubMed  Google Scholar 

  91. Hill RA (2007) Marine natural products. Annu Rep Prog Chem Sect B: Org Chem 102:123–137. doi:10.1039/B515100G

    Article  Google Scholar 

  92. Nguyen XC, Longeon A, Pham VC, Urvois F, Bressy C, Trinh TT, Nguyen HN, Phan VK, Chau VM, Briand JF, Bourguet-Kondracki ML (2013) Antifouling 26, 27-cyclosterols from the Vietnamese marine sponge Xestospongia testudinaria. J Nat Prod 76:1313–1318. doi:10.1021/np400288j

    Article  CAS  PubMed  Google Scholar 

  93. Youssef DTA (2005) Hyrtioerectines A − C, Cytotoxic Alkaloids from the Red Sea Sponge Hyrtios erectus. J Nat Prod 68:1416–1419. doi:10.1021/np050142c

    Article  CAS  PubMed  Google Scholar 

  94. Youssef DTA, Shaala LA, Asfour HZ (2013) Bioactive compounds from the Red Sea Marine sponge Hyrtios species. Mar Drugs 11:1061–1070. doi:10.3390/md11041061

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  95. Zhou X, Lu Y, Lin X, Yang B, Yang X, Liu Y (2011) Brominated aliphatic hydrocarbons and sterols from the sponge Xestospongia testudinaria with their bioactivities. Chem Phys Lipids 164:703–706. doi:10.1016/j.chemphyslip.2011.08.002

    Article  CAS  PubMed  Google Scholar 

  96. Patel K, Laville R, Martin MT, Tilvi S, Moriou C, Gallard JF, Ermolenko L, Debitus C, Al-Mourabit A (2010) Unprecedented stylissazoles A-C from Stylissa carteri: another dimension for marine pyrrole-2-aminoimidazole metabolite diversity. Angew Chem Int Edit 49:4775–4779. doi:10.1002/anie.201000444

    Article  CAS  Google Scholar 

  97. Rohde S, Gochfeld D, Ankisetty S, Avula B, Schupp P, Slattery M (2012) Spatial variability in secondary metabolites of the indo-pacific sponge Stylissa massa. J Chem Ecol 38:463–475. doi:10.1007/s10886-012-0124-8

    Article  CAS  PubMed  Google Scholar 

  98. Wang X, Morinaka BI, Molinski TF (2014) Structures and solution conformational dynamics of stylissamides G and H from the Bahamian sponge Stylissa caribica. J Nat Prod 77:625–630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  99. Yamaguchi M, Miyazaki M, Kodrasov MP, Rotinsulu H, Losung F, Mangindaan REP, de Voogd NJ, Yokosawa H, Nicholson B, Tsukamoto S (2013) Spongiacidin C, a pyrrole alkaloid from the marine sponge Stylissa massa, functions as a USP7 inhibitor. Bioorg Med Chem Lett 23:3884–3886. doi:10.1016/j.bmcl.2013.04.066

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Portuguese Foundation for Science and Technology (FCT) under grant PTDC/AAC-AMB/115304/2009 (LESS CORAL) and a PhD Fellowship SFRH/BD/33391/2008. Samples were collected under a research permit issued by the Indonesian State Ministry for Research and Technology (Kementerian Riset Dan Teknologi Republik Indonesia (RISTEK)). We thank the Indonesian Institute of Sciences (PPO-LIPI) for their support and especially Yos Tuti.

Author information

Authors and Affiliations

  1. Departamento de Biologia, Centro de Estudos do Ambiente e do Mar (CESAM), Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Daniel F. R. Cleary, Ana R. M. Polónia, Rossana Freitas & Newton C. M. Gomes

  2. Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA, Leiden, The Netherlands

    Nicole J. de Voogd

Authors
  1. Daniel F. R. Cleary
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicole J. de Voogd
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana R. M. Polónia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rossana Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Newton C. M. Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel F. R. Cleary.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

(PDF 113 kb)

Online Resource 2

Stacked barplot showing the relative abundances of the nine most abundant phyla sampled from the six biotopes, a) S. carteri, b) S. massa, c) X. testudinaria, d) H. erectus, e) Sediment and f) Seawater. The site codes (x axis) are Lae: Lae Lae, Sam: Samalona, Kud: Kudingkareng Keke, Bak: Bone Baku and Lan: Langkai (PDF 7.10 kb)

Online Resource 3

List of most abundant OTUs (>300 sequences) including OTU-numbers; total sequences (Sum) and the subtotals for samples from seawater (Wt); sediment (Sd); S. massa (Sm); S. carteri (Sc); X. testudinaria (Xt); H. erectus (He); taxonomic affiliation of OTU, GenBank GenInfo sequence identifiers (GI) of closely related organisms identified using BLAST; sequence identity (Sq ident) of these organisms with our representative OTU sequences; isolation source (Source) of closely related organisms identified using BLAST; location where the isolation source was sampled (Location). (XLS 18 kb)

Online Resource 4

Maximum Likelihood phylogenetic tree (16S rRNA gene sequences) of the most dominant OTUs(Table 1) assigned to the phylum Proteobacteria and their cultured closest relatives (gi = GeneBank sequence identification number). Symbols represent samples from seawater (Wt), sediment (Sd), S. massa (Sm), S. carteri (Sc), X. testudinaria (Xt) and H. erectus (He). Bootstrap values generated from 500 replicates. Bootstrap values lower than 50 % were omitted. For the analysis, selected 16S rRNA gene sequences of the most dominant OTUs (≥300 sequences) and their cultured closest relatives in GenBank [http://www.ncbi.nlm.nih.gov/] were aligned using ClustalW and a phylogenetic analysis conducted using MEGA 6 software (http://www.megasoftware.net/) (Tamura et al., 2011). Phylogenetic trees were constructed according to the maximum-likelihood statistical method using the general time reversible (GTR) model with a discrete Gamma distribution (5 categories (+G, parameter = 0.4305). In the results, we present a bootstrap consensus tree based on 500 replicates. The bootstrap value is shown next to each branch when this exceeds 49 %. This value represents the percentage of replicate trees in which the associated taxa clustered together. For tree inference we used the nearest neighbor interchange (NNI) heuristic method and automatic initial tree selection. (PDF 18 kb)

Online Resource 5

Maximum Likelihood phylogenetic tree (16S rRNA gene sequences) of the most dominant OTUs(Table 1) assigned to the non-proteobacterial phyla and their cultured closest relatives (gi = GeneBank sequence identification number). Symbols represent samples from seawater (Wt), sediment (Sd), S. massa (Sm), S. carteri (Sc), X. testudinaria (Xt) and H. erectus (He). Bootstrap values generated from 500 replicates. Bootstrap values lower than 50 % were omitted. (PDF 10 kb)

Online Resource 6

Stacked bar plots showing the estimated gene count (Y axis) of a set of KOs and the contribution of selected orders to the gene count; unclassified OTUs at the order level and OTUs belonging to all other orders are pooled and indicated by ‘Other’. a) K00087 (xanthine dehydrogenase molybdenum-binding subunit), b) K03409 (chemotaxis protein CheX), c) K04561 (nitric oxide reductase) and d) K10535 (hydroxylamine oxidase) for all samples (X axis). (PDF 7 kb)

Online Resource 7

Stacked bar plots showing the estimated gene count (Y axis) of a set of KOs and the contribution of selected orders to the gene count; unclassified OTUs at the order level and OTUs belonging to all other orders are pooled and indicated by ‘Other’. a) K05522 (endonuclease VIII), b) K07239 (heavy metal exporter), c) K07334 (proteic killer suppression protein) and d) K07665 (copper resistance phosphate regulon response regulator CusR) for all samples (X axis). (PDF 9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cleary, D.F.R., de Voogd, N.J., Polónia, A.R.M. et al. Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia. Microb Ecol 70, 889–903 (2015). https://doi.org/10.1007/s00248-015-0632-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0632-5

Keywords

Search

Navigation