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Compositional analysis of bacterial communities in seawater, sediment, and sponges in the Misool coral reef system, Indonesia

  • Daniel Francis Richard Cleary
  • Ana Rita Moura Polónia
  • Leontine E. Becking
  • Nicole Joy de Voogd
  • Purwanto
  • Helder Gomes
  • Newton Carlos Marcial Gomes
Original Paper

Abstract

Sponge species have been deemed high microbial abundance (HMA) or low microbial abundance (LMA) based on the composition and abundance of their microbial symbionts. In the present study, we evaluated the richness and composition of bacterial communities associated with one HMA sponge (Xestospongia testudinaria; Demospongiae: Haplosclerida: Petrosiidae), one LMA sponge (Stylissa carteri; Demospongiae: Scopalinida - Scopalinidae), and one sponge with a hitherto unknown microbial community (Aaptos suberitoides; Demospongiae: Suberitida: Suberitidae) inhabiting the Misool coral reef system in the West Papua province of Indonesia. The bacterial communities of these sponge species were also compared with seawater and sediment bacterial communities from the same coastal coral reef habitat. Using a 16S rRNA gene barcoded pyrosequencing approach, we showed that the most abundant phylum overall was Proteobacteria. The biotope (sponge species, sediment or seawater) explained almost 84% of the variation in bacterial composition with highly significant differences in composition among biotopes and a clear separation between bacterial communities from seawater and S. carteri; X. testudinaria and A. suberitoides and sediment. The Chloroflexi classes SAR202 and Anaerolineae were most abundant in A. suberitoides and X. testudinaria and both of these species shared several OTUs that were largely absent in the remaining biotopes. This suggests that A. suberitoides is a HMA sponge. Although similar, the bacterial communities of S. carteri and seawater were compositionally distinct. These results confirm compositional differences between sponge and non-sponge biotopes and between HMA and LMA sponges.

Keywords

Aaptos suberitoides Microbial abundance Stylissa Carteri 16S rRNA gene, Xestospongia testudinaria 

Notes

Acknowledgements

Funding for the present study was provided by grants to the projects LESS CORAL (PTDC/AAC-AMB/115304/2009), Ecotech-Sponge (PTDC/BIA-MIC/6473/2014 - POCI-01-0145-FEDER-016531) and to CESAM (UID/AMB/50017 – POCI-01-0145-FEDER-007638) by FCT/MEC through national funds and co-funding by FEDER within the PT2020 Partnership Agreement and Compete 2020. The Netherlands Organisation for Scientific Research provided funding to LEB through the grant RUBICON #825.12.007 and VENI#863.14.020. We are grateful for the support in the field by Misool Eco Resort, Andy Miners, Dadi, Christiaan de Leeuw, and The Nature Conservancy.

Compliance with ethical standards

Funding

Funding for the present study was provided by grants to the projects LESS CORAL (PTDC/AAC-AMB/115304/2009), Ecotech-Sponge (PTDC/BIA-MIC/6473/2014 - POCI-01-0145-FEDER-016531) and to CESAM (UID/AMB/50017 – POCI-01-0145-FEDER-007638) by FCT/MEC through national funds and co-funding by FEDER within the PT2020 Partnership Agreement and Compete 2020. The Netherlands Organisation for Scientific Research provided funding to LEB through the grant RUBICON #825.12.007 and VENI#863.14.020. Fieldwork was supported by Ristek and LIPI, Indonesia.

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

12526_2017_697_MOESM1_ESM.pdf (99 kb)
ESM 1 (PDF 99 kb)
12526_2017_697_MOESM2_ESM.pdf (42 kb)
ESM 2 Species accumulation curves as a function of the number of sequences using resampling of bacterial 16S rRNA gene sequences from S. carteri (Sc), A. suberitoides (Ap), X. testudinaria (Xt), sediment (Sd) and seawater (Wt). (PDF 41 kb)
12526_2017_697_MOESM3_ESM.pdf (6 kb)
ESM 3 Stacked barplots showing the relative abundance of the 8 most abundant phyla sampled from the five biotopes. (a) S. carteri, (b) A. suberitoides, (c) X. testudinaria, (d) sediment and (e) seawater. The samples codes (X-axis) represent samples sampling sites Mer1, Mer2, Mer5, Ms17 and Ms31. (PDF 6 kb)

References

  1. Akiyama T, Takada K, Oikawa T, Matsuura N, Ise Y, Okada S, Matsunaga S (2013) Stimulators of adipogenesis from the marine sponge Xestospongia testudinaria. Tetrahedron 69:6560–6564. doi: 10.1016/j.tet.2013.06.007 CrossRefGoogle Scholar
  2. Allen GR (2008) Conservation hotspots of biodiversity and endemism for indo-Pacific coral reef fishes. Aquat Conserv Mar Freshwat Ecosyst 18:541–556CrossRefGoogle Scholar
  3. Allen GR, Erdmann MV (2009) Reef fishes of the bird’s head peninsula, West Papua, Indonesia. Check List 5:587–628CrossRefGoogle Scholar
  4. Aoki S, Kong D, Suna H, Sowa Y, Sakai T, Setiawan A, Kobayashi M (2006) Aaptamine, a spongean alkaloid, activates p21 promoter in a p53-independent manner. Biochem Bioph Res Commun 342:101–106. doi: 10.1016/j.bbrc.2006.01.119 CrossRefGoogle Scholar
  5. Becking LE, de Leeuw C, Vogler C (2014) Newly discovered "jellyfish lakes" in Misool, Raja Ampat, Papua, Indonesia. Mar Biodivers 45:597–598CrossRefGoogle Scholar
  6. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  7. Borchiellini C, Manuel M, Alivon E, Boury-Esnault N, Vacelet J, Le Parco Y (2001) Sponge paraphyly and the origin of Metazoa. J Evol Biol 14:171–179. doi: 10.1046/j.1420-9101.2001.00244.x CrossRefGoogle Scholar
  8. Bruno JF, Selig ER (2007) Regional decline of coral cover in the indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:e711CrossRefPubMedPubMedCentralGoogle Scholar
  9. Campbell AG, Schwientek P, Vishnivetskaya T, Woyke T, Levy S, Beall CJ, Griffen A, Leys E, Podar M (2014) Diversity and genomic insights into the uncultured Chloroflexi from the human microbiota. Environ Microbiol 16:2635–2643. doi: 10.1111/1462-2920.12461 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Capone DG, Dunham SE, Horrigan SG, Duguay LE (1992) Microbial nitrogen transformations in unconsolidated coral reef sediments. Mar Ecol Prog Ser 80:75–88CrossRefGoogle Scholar
  11. Cleary DFR (2003) An examination of scale of assessment, logging and ENSO-induced fires on butterfly diversity in Borneo. Oecologia 135:313–321. doi: 10.1007/s00442-003-1188-5 CrossRefPubMedGoogle Scholar
  12. Cleary DFR, Becking LE, de 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. doi: 10.1111/1574-6941.12135 CrossRefPubMedGoogle Scholar
  13. Cleary DFR, de Voogd NJ, Polónia ARM, Freitas R, Gomes NCM (2015) Composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in an Indonesian coral reef environment. Microb Ecol 70:889–903CrossRefPubMedGoogle Scholar
  14. Coelho FJ, Cleary DFR, Rocha RJ, Calado R, Castanheira JM, Rocha et al (2015) Unraveling the interactive effects of climate change and oil contamination on laboratory-simulated estuarine benthic communities. Glob Chang Biol 21:1871–1886CrossRefPubMedGoogle Scholar
  15. 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 109:17995–17999CrossRefPubMedPubMedCentralGoogle Scholar
  16. de Goeij JM, van Oevelen D, Vermeij MJ, Osinga R, Middelburg JJ, de Goeij AF, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110. doi: 10.1126/science.1241981 CrossRefPubMedGoogle Scholar
  17. de Voogd NJ, Cleary DFR (2008) An analysis of sponge diversity and distribution at three taxonomic levels in the Thousand Islands/Jakarta Bay reef complex, West-java, Indonesia. Mar Ecol 29:205–215CrossRefGoogle Scholar
  18. de Voogd NJ, Cleary DFR (2009) Variation in sponge composition among Singapore reefs. Raffles B Zool Suppl 22:59–67Google Scholar
  19. de Voogd NJ, Cleary DFR, Hoeksema BW, Noor A, van Soest RWM (2006) Sponge beta diversity in the Spermonde archipelago, SW Sulawesi, Indonesia. Mar Ecol Prog Ser 309:131–142. doi: 10.3354/meps309131 CrossRefGoogle Scholar
  20. de Voogd NJ, Cleary DFR, Polónia ARM, Gomes NCM (2015) Bacterial community composition and predicted functional ecology of sponges, sediment and seawater from the thousand islands reef complex, West java, Indonesia. FEMS Microbiol Ecol 91:1–12. doi: 10.1093/femsec/fiv019 CrossRefGoogle Scholar
  21. Ebada SS, Linh MH, Longeon A, de Voogd NJ, Durieu E, Meijer L, Bourguet-Kondracki ML, Singab AN, Müller WE, Proksch P (2015) Dispacamide E and other bioactive bromopyrrole alkaloids from two Indonesian marine sponges of the genus Stylissa. Nat Prod Res 29:231–238. doi: 10.1080/14786419.2014.947496 CrossRefPubMedGoogle Scholar
  22. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998CrossRefPubMedGoogle Scholar
  23. Edgar R, Haas B, Clemente J, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  24. Faulkner DJ (2002) Marine natural products. Nat Prod Rep 19:1–48. doi: 10.1039/b009029h PubMedGoogle Scholar
  25. Flatt PM, Gautschi JT, Thacker RW, Musafija-Girt M, Crews P, Gerwick WH (2005) Identification of the cellular site of polychlorinated peptide biosynthesis in the marine sponge Dysidea (Lamellodysidea) herbacea and symbiotic cyanobacterium Oscillatoria spongeliae by CARD-FISH analysis. Mar Biol 147:761–774. doi: 10.1007/s00227-005-1614-9 CrossRefGoogle Scholar
  26. Freeman CJ, Thacker RW (2011) Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr 56:1577–1586. doi: 10.4319/lo.2011.56.5.1577 CrossRefGoogle Scholar
  27. Giles C, 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 83:232–241CrossRefPubMedGoogle Scholar
  28. Giles EC, Saenz-Agudelo P, Hussey NE, Ravasi T, Berumen ML (2015) Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea. Ecol Evol 5:2487–2502. doi: 10.1002/ece3.1511 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Glöckner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726PubMedPubMedCentralGoogle Scholar
  30. Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Schupp P, Pawlik JR et al (2014) The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull 227:78–88CrossRefPubMedGoogle Scholar
  31. Gomes NCM, Heuer H, Schönfeld J, Costa RS, Mendonça-Hagler LCS et al (2001) Bacterial diversity of the rhisosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180. doi: 10.1023/A:1010350406708 CrossRefGoogle Scholar
  32. Gomes NCM, Cleary DFR, Pinto FN, Egas C, Almeida A, Cunha A, Mendonça-Hagler LCS, Smalla K (2010) Taking root: enduring effect of rhisosphere bacterial colonization in mangroves. PLoS One 5:e14065-aCrossRefGoogle Scholar
  33. Grantham HS, Agostini VN, Wilson J, Mangubhai S, Hidayat N, Muljadi A et al (2013) A comparison of zoning analyses to inform the planning of a marine protected area network in Raja Ampat. Indones Mar Policy 38:184–194CrossRefGoogle Scholar
  34. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Muller WE (ed) Sponges (Porifera). Springer-Verlag, Heidelberg, pp 59–88CrossRefGoogle Scholar
  35. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177CrossRefPubMedGoogle Scholar
  36. Huang YM, de Voogd NJ, Cleary DFR, Li TH, Mok HK, Ueng JP (2016) Biodiversity pattern of Subtidal sponges (Porifera: Demospongiae) in the Penghu archipelago (Pescadores), Taiwan. J Mar Biol Assoc UK 96:417–427. doi: 10.1017/S002531541500017X CrossRefGoogle Scholar
  37. Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR, Williams KH, Tringe SG. Banfield JF (2013) Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1:1 - 22. doi:  10.1186/2049-2618-1-22.
  38. Jin M, Zhao W, Zhang Y, Kobayashi M, Duan H, Kong D (2011) Antiproliferative effect of aaptamine on human chronic myeloid leukemia K562 cells. Int J Mol Sci 12:7352–7359. doi: 10.3390/ijms12117352 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kamke J, Taylor MW, Schmitt S (2010) Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME J 4:498–508. doi: 10.1038/ismej.2009.143 CrossRefPubMedGoogle Scholar
  40. Larghi EL, Obrist BV, Kaufman TS (2008) A formal total synthesis of the marine alkaloid aaptamine. Tetrahedron 64:5236–5245. doi: 10.1016/j.tet.2008.03.036 CrossRefGoogle Scholar
  41. 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 CrossRefPubMedGoogle Scholar
  42. Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. doi: 10.1007/s004420100716 CrossRefGoogle Scholar
  43. Li CW, Chen JY, Hua TE (1998) Precambrian sponges with cellular structures. Science 279:879–882CrossRefPubMedGoogle Scholar
  44. Liang LF, Wang T, Cai YS, He WF, Sun P, Li YF, Huang Q, Taglialatela-Scafati O, Wang HY, Guo YW (2014) Brominated polyunsaturated lipids from the Chinese sponge Xestospongia testudinaria as a new class of pancreatic lipase inhibitors. Eur J Med Chem 79:290–297. doi: 10.1016/j.ejmech.2014.04.003 CrossRefPubMedGoogle Scholar
  45. Liu C, Tang X, Li P, Li G (2012) Suberitine A-D, four new cytotoxic dimeric aaptamine alkaloids from the marine sponge Aaptos suberitoides. Org Lett 14:1994–1997. doi: 10.1021/ol3004589 CrossRefPubMedGoogle Scholar
  46. Mangubhai S, Erdmann MV, Wilson JR, Huffard CL, Ballamu F, Hidayat NI, Hitipeuw C, Lazuardi ME et al (2012) Papuan Bird’s head seascape: emerging threats and challenges in the global center of marine biodiversity. Mar Pollut Bull 64:2279–2295CrossRefPubMedGoogle Scholar
  47. McMurray SE, Blum JE, Pawlik JR (2008) Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida keys. Mar Biol 155:159–171CrossRefGoogle Scholar
  48. Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233CrossRefGoogle Scholar
  49. 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. doi: 10.1111/mec.12365 CrossRefPubMedGoogle Scholar
  50. 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. doi: 10.1128/AEM.05285-11 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Montalvo NF, Davis J, Vicente J, Pittiglio R, Ravel J, Hill RT (2014) Integration of culture-based and molecular analysis of a complex sponge-associated bacterial community. PLoS One 9:e90517CrossRefPubMedPubMedCentralGoogle Scholar
  52. Morrow C, Cárdenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front Zool 12:1–7CrossRefGoogle Scholar
  53. Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454PubMedGoogle Scholar
  54. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Wagner H (2009) Vegan: community ecology package. R Packag Vers 1:15–14 Retrieved from http://www.cran.r-project.org/package=vegan Google Scholar
  55. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJ, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958CrossRefPubMedGoogle Scholar
  56. Pham NB, Butler MS, Hooper JNA, Moni RW, Quinn RJ (1999) Isolation of xestosterol esters of brominated acetylenic fatty acids from the marine sponge Xestospongia testudinaria. J Nat Prod 62:1439–1442CrossRefPubMedGoogle Scholar
  57. Pham CD, Hartmann R, Müller WEG, de Voogd NJ, Lai D, Proksch P (2013) Aaptamine derivatives from the indonesian sponge Aaptos suberitoides. J Nat Prod 76:103–106. doi: 10.1021/np300794b CrossRefPubMedGoogle Scholar
  58. Polónia ARM, Cleary DFR, Freitas R, de Voogd NJ, Gomes NCM (2014) 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 CrossRefGoogle Scholar
  59. Prentice ML, Hope GS (2007) Climate of Papua. In: Marshall AJ, Beehler BM (eds) The ecology of Papua: part one. Periplus, Singapore, pp 177–196Google Scholar
  60. Roberts CM, McClean CJ, Veron JE, Hawkins JP, Allen GR, McAllister DE et al (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284CrossRefPubMedGoogle Scholar
  61. 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 CrossRefPubMedGoogle Scholar
  62. Rützler K (2004) Sponges on coral reefs: a community shaped by competitive cooperation. Bollettino dei Musei e degli Instituti Biologici dell’Universita Di Genova 68:85–148Google Scholar
  63. Schlappy ML, Schottner SI, Lavik G, Kuypers MM, de Beer D, Hoffmann F (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157:593–602CrossRefPubMedGoogle Scholar
  64. Schmitt S, Deines P, Behman F, Wagner M, Taylor MW (2011) Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges. FEMS Microbiol Ecol 78:497–510CrossRefPubMedGoogle Scholar
  65. van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, de Voogd NJ, Santodomingo N, Vanhoorne B, Kelly M, Hooper JNA (2012) Global diversity of sponges (Porifera). PLoS One 7:1–23Google Scholar
  66. Swierts T, Peijnenburg KTCA, de Leeuw C, Cleary DFR, Setiawan E, Wörheide G, Erpenbeck D, de Voogd NJ (2013) Lock, stock and two different barrels: comparing the genetic composition of morphotypes of the indo-Pacific sponge Xestospongia testudinaria. PLoS One 8:1–12. doi: 10.1371/journal.pone.0074396 CrossRefGoogle Scholar
  67. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725-2729Google Scholar
  68. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347. doi: 10.1128/MMBR.00040-06 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Tsukamoto S, Yamanokuchi R, Yoshitomi M, Sato K, Ikeda T, Rotinsulu H, Mangindaan REP, de Voogd NJ, van Soest RWM, Yokosawa H (2010) Aaptamine, an alkaloid from the sponge Aaptos suberitoides, functions as a proteasome inhibitor. Bioorg Med Chem Lett 20:3341–3343. doi: 10.1016/j.bmcl.2010.04.029 CrossRefPubMedGoogle Scholar
  70. 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
  71. Varela MM, van Aken HM, Herndl GJ (2008) Abundance and activity of Chloroflexi-type SAR202 bacterioplankton in the meso- and bathypelagic waters of the (sub)tropical Atlantic. Environ Microbiol 10:1903–1911. doi: 10.1111/j.1462-2920.2008.01627.x CrossRefPubMedGoogle Scholar
  72. Vaz-Moreira I, Egas C, Nunes OC, Manaia CM (2011) Culture-dependent and culture-independent diversity surveys target different bacteria: a case study in a freshwater sample. Antonie Van Leeuwenhoek 100:245–257CrossRefPubMedGoogle Scholar
  73. 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 CrossRefPubMedGoogle Scholar
  74. Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679CrossRefPubMedGoogle Scholar
  75. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214CrossRefPubMedGoogle Scholar
  76. Zhou J, He Q, Hemme CL, Mukhopadhyay A, Hillesland K, Zhou A, He Z, Van Nostrand JD, Hazen TC, Stahl DA, Wall JD, Arkin AP (2011) How sulphate-reducing microorganisms cope with stress: lessons from systems biology. Nat Rev Microbiol 9:452–466. doi: 10.1038/nrmicro2575 CrossRefPubMedGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Daniel Francis Richard Cleary
    • 1
  • Ana Rita Moura Polónia
    • 1
  • Leontine E. Becking
    • 2
    • 3
    • 4
  • Nicole Joy de Voogd
    • 2
  • Purwanto
    • 5
  • Helder Gomes
    • 1
  • Newton Carlos Marcial Gomes
    • 1
  1. 1.Department of Biology, CESAMUniversidade de AveiroAveiroPortugal
  2. 2.Marine Biodiversity, Naturalis Biodiversity CenterLeidenThe Netherlands
  3. 3.Marine Animal EcologyWageningen URWageningenThe Netherlands
  4. 4.Department of Environmental Science, Policy, and ManagementUniversity of California BerkeleyBerkeleyUSA
  5. 5.Department of Fisheries and Marine ScienceUniversity of DiponegoroSemarangIndonesia

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