Skip to main content

Advertisement

SpringerLink
Log in

Bacterial Communities Inhabiting the Sponge Biemna fortis, Sediment and Water in Marine Lakes and the Open Sea

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

Abstract

Marine lakes are small bodies of landlocked seawater that are isolated from the open sea and have been shown to house numerous rare and unique taxa. The environmental conditions of the lakes are also characterised by lower pH and salinity and higher temperatures than generally found in the open sea. In the present study, we used a 16S rRNA gene barcoded pyrosequencing approach and a predictive metagenomic approach (PICRUSt) to examine bacterial composition and function in three distinct biotopes (sediment, water and the sponge species Biemna fortis) in three habitats (two marine lakes and the open sea) of the Berau reef system, Indonesia. Both biotope and habitat were significant predictors of higher taxon abundance and compositional variation. Most of the variation in operational taxonomic unit (OTU) composition was related to the biotope (42% for biotope alone versus 9% for habitat alone and 15% combined). Most OTUs were also restricted to a single biotope (1047 for B. fortis, 6120 for sediment and 471 for water). Only 98 OTUs were shared across all three biotopes. Bacterial communities from B. fortis, sediment and water samples were, however, also distinct in marine lake and open sea habitats. This was evident in the abundance of higher bacterial taxa. For example, the phylum Cyanobacteria was significantly more abundant in samples from marine lakes than from the open sea. This difference was most pronounced in the sponge B. fortis. In line with the compositional differences, there were pronounced differences in predicted relative gene count abundance among biotopes and habitats. Of particular interest was the predicted enrichment in B. fortis from the marine lakes for pathways including DNA replication and repair and the glutathione metabolism. This may facilitate adaptation of host and microbes to life in ‘stressful’ low pH, low salinity and/or high temperature environments such as those encountered in marine lakes.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Becking LE, Cleary DFR, De Voogd NJ (2013) Sponge species composition, abundance, and cover in marine lakes and coastal mangroves in Berau, Indonesia. Mar. Ecol. Prog. Ser. 481:105–120. https://doi.org/10.3354/meps10155

    Article  Google Scholar 

  2. Dawson MN, Hamner WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. P Natl Acad Sci USA 102:9235–9240. https://doi.org/10.1073/pnas.0503635102

    Article  CAS  Google Scholar 

  3. Becking LE, Renema W, Santodomingo NK, Hoeksema BW, Tuti Y, De Voogd NJ (2011) Recently discovered landlocked basins in Indonesia reveal high habitat diversity in anchialine systems. Hydrobiologia 677:89–105. https://doi.org/10.1007/s10750-011-0742-0

    Article  CAS  Google Scholar 

  4. Becking LE, De Leeuw C, Vogler C (2014) Newly discovered “jellyfish lakes” in Misool, Raja Ampat, Papua, Indonesia. Mar. Biodivers. 45:597–598. https://doi.org/10.1007/s12526-014-0268-6

    Article  Google Scholar 

  5. Cleary DFR, Becking LE, Pires ACC, de Voogd NJ, Egas C, Gomes NCM (2013) Habitat and host related variation in sponge bacterial communities in Indonesian coral reefs and marine lakes. FEMS Microbiol. Ecol. 85:465–482. https://doi.org/10.1111/1574-6941.12135

    Article  PubMed  CAS  Google Scholar 

  6. Cleary DFR, Becking LE, Polónia ARM, Freitas RM, Gomes NCM (2015) Composition and predicted functional ecology of mussel-associated bacteria in Indonesian marine lakes. A Van Leeuw J Microb 107:821–834. https://doi.org/10.1007/s10482-014-0375-1

    Article  Google Scholar 

  7. Cleary DFR, Becking LE, Polónia ARM, Freitas R, Gomes NCM (2016) Jellyfish-associated bacterial communities and bacterioplankton in Indonesian Marine lakes. FEMS Microbiol Ecol 92:fiw064. https://doi.org/10.1093/femsec/fiw064

    Article  PubMed  CAS  Google Scholar 

  8. Cleary DFR, Polónia ARM (2017) Bacterial and archaeal communities inhabiting mussels, sediment and water in Indonesian anchialine lakes. A Van Leeuw J Microb. doi: https://doi.org/10.1007/s10482-017-0944-1

  9. Caston CB, Nowlin WH, Gaulke A, Vanni MJ (2009) The relative importance of heterotrophic bacteria to pelagic ecosystem dynamics varies with reservoir trophic state. Limnol. Oceanogr. 54:2143–2156

    Article  Google Scholar 

  10. Blunt JW, Munro MHG (1998) MarinLit. A database of the literature on marine natural products for use on a Macintosh computer prepared and maintained by the Marine Chemistry Group Department of Chemistry. University of Canterbury, Canterbury, New Zealand

    Google Scholar 

  11. Van Soest RWM, Braekman JC (1999) Chemosystematics of Porifera: a review. Mem Queensl Mus 44:569–598

    Google Scholar 

  12. Faulkner DJ, Harper MK, Haygood MG, Salomon CE, Schmidt EW (2000) Symbiotic bacteria in sponges: sources of bioactive substances. In: Fusetani N (ed) Drugs from the sea. Karger, Basel, Switzerland, pp 107–119

    Chapter  Google Scholar 

  13. Sipkema D, Franssen MCR, Osinga R, Tramper J, Wijffels RH (2005) Marine sponges as pharmacy. Mar. Biotechnol. 7:142–162. https://doi.org/10.1007/s10126-004-0405-5

    Article  PubMed  CAS  Google Scholar 

  14. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol R 71:295–347. https://doi.org/10.1128/MMBR.00040-06

    Article  CAS  Google Scholar 

  15. Unson MD, Holland ND, Faulkner DJ (1994) A brominated secondary metabolite synthesized by the cyanobacterial symbiont of a marine sponge and accumulation of a crystalline metabolite in the sponge tissue. Mar Biol 119:1–11. https://doi.org/10.1007/BF00350100

    Article  CAS  Google Scholar 

  16. Friedrich AB, Fischer I, Proksch P, Hacker H, Hentschel U (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol. Ecol. 38:105–113. https://doi.org/10.1111/j.1574-6941.2001.tb00888.x

    Article  CAS  Google Scholar 

  17. Sacristán-Soriano O, Banaigs B, Casamayor EO, Becerro MA (2011) Exploring the links between natural products and bacterial assemblages in the sponge Aplysina aerophoba. Appl. Environ. Microbiol. 77:862–870. https://doi.org/10.1128/AEM.00100-10

    Article  PubMed  CAS  Google Scholar 

  18. Currie DJ, Kalff JK (1984) The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in freshwater. Limnol. Oceanogr. 29:311–321

    Article  CAS  Google Scholar 

  19. Danger M, Umarou CO, Benest D, Lacroix G (2007) Bacteria can control stoichiometry and nutrient limitation of phytoplankton. Funct. Ecol. 21:202–210. https://doi.org/10.1111/j.1365-2435.2006.01222.x

    Article  Google Scholar 

  20. Reiswig HM (1975) Bacteria as food for temperate-water marine demosponges. Can. J. Zool. 53:582–589

    Article  Google Scholar 

  21. Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155–189. https://doi.org/10.1146/annurev.micro.59.030804.121041

    Article  PubMed  CAS  Google Scholar 

  22. Macdonald TT, Monteleone G (2005) Immunity, inflammation, and allergy in the gut. Science 307:1920–1925. https://doi.org/10.1126/science.1106442

    Article  PubMed  CAS  Google Scholar 

  23. Scarborough CL, Ferrari J, Godfray HC (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781. https://doi.org/10.1126/science.1120180

    Article  PubMed  CAS  Google Scholar 

  24. Hurst GD, Werren JH (2001) The role of selfish genetic elements in eukaryotic evolution. Nat Rev Genet 2:597–606. https://doi.org/10.1038/35084545

    Article  PubMed  CAS  Google Scholar 

  25. Wilkinson CR (1978) Microbial association in sponges. II. Numerical analysis of sponge and water bacterial populations. Mar. Biol. 49:169–176

    Article  Google Scholar 

  26. Hoffmann F, Larsen O, Rapp HT, Osinga R (2005) Oxygen dynamics in choanosomal sponge explants. Mar. Biol. Res. 1:160–163. https://doi.org/10.1080/17451000510019006

    Article  Google Scholar 

  27. Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schlaeppy ML, Schleper C, Kuypers MMM (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

    Article  PubMed  CAS  Google Scholar 

  28. Holmes B, Blanch H (2007) Genus-specific associations of marine sponges with group I crenarchaeotes. Mar. Biol. 150:759–772. https://doi.org/10.1007/s00227-006-0361-x

    Article  Google Scholar 

  29. Carpenter EJ, Foster RA (2002) Marine cyanobacterial symbioses. In Cyanobacteria in Symbiosis. Springer, Netherlands, pp 11–17

    Google Scholar 

  30. Wilkinson C, Fay P (1979) Nitrogen fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527–529. https://doi.org/10.1038/279527a0

    Article  CAS  Google Scholar 

  31. Fiore CL, Jarett JK, Olson ND, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends in microbiol 18:455–463

    Article  CAS  Google Scholar 

  32. Ribes M, Dziallas C, Coma R, Riemann L (2015) Microbial diversity and putative diazotrophy in high- and low-microbial-abundance Mediterranean sponges. Appl. Environ. Microbiol. 81:5683–5693. https://doi.org/10.1128/AEM.01320-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Holthuis LB (1973) Caridean shrimps found in land-locked saltwater pools at four indo-west pacific localities (Sinai Peninsula, Funafuti Atoll, Maui and Hawaii Islands), with the description of one new genus and four new species. Zool Verhandel 128:1–48

    Google Scholar 

  34. Maciolek J (1983) Distribution and biology of Indo-Pacific insular hypogeal shrimps. B Mar Sci 33:606–618

    Google Scholar 

  35. Tomascik T, Mah AJ (1994) The ecology of ‘Halimeda open sea’: an anchialine open sea of a raised atoll, Kakaban Island, East Kalimantan, Indonesia. Tropical Biodiversity 2:385–399

    Google Scholar 

  36. Massin C, Tomascik T (1996) Two new holothurians (Echinodermata: Holothuroidea) from an anchialine open sea of an uplifted atoll, Kakaban Island, East Kalimantan, Indonesia. Raffles B Zool 44:157–172

    Google Scholar 

  37. Gros E, Martin MT, Sorres J, Moriou C, Vacelet J, Frederich M et al (2015) Netamines O–S, five new tricyclic guanidine alkaloids from the Madagascar sponge Biemna laboutei, and their antimalarial activities. Chem. Biodivers. 12:1725–1733. https://doi.org/10.1002/cbdv.201400350

    Article  PubMed  CAS  Google Scholar 

  38. Moran DAP, Takada K, Ise Y, Bontemps N, Davis RA, Furihata K et al (2015) Two cell differentiation inducing pyridoacridines from a marine sponge Biemna sp. and their chemical conversions. Tetrahedron 71:5013–5018. https://doi.org/10.1016/j.tet.2015.05.070

    Article  CAS  Google Scholar 

  39. Youssef DT, Badr JM, Shaala LA, Mohamed GA, Bamanie FH (2015) Ehrenasterol and biemnic acid; new bioactive compounds from the Red Sea sponge Biemna ehrenbergi. Phytochem. Lett. 12:296–301. https://doi.org/10.1016/j.phytol.2015.04.024

    Article  CAS  Google Scholar 

  40. Ilan M, Abelson A (1995) The life of a sponge in a sandy open sea. Biol. Bull. 189:363–369. https://doi.org/10.2307/1542154

    Article  PubMed  CAS  Google Scholar 

  41. 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. 227:78–88. https://doi.org/10.1086/BBLv227n1p78

    Article  PubMed  Google Scholar 

  42. Morrow C, Cárdenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front in Zool 12:7. https://doi.org/10.1186/s12983-015-0099-810.1086/BBLv227n1p78

    Article  Google Scholar 

  43. 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. https://doi.org/10.1038/ismej.2012.47

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Gomes NCM, Heuer H, Schönfeld J, Costa R, Mendonca-Hagler L, Smalla K (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. https://doi.org/10.1007/978-94-010-0566-1_17

    Article  CAS  Google Scholar 

  45. 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. 89:670–679

    Article  PubMed  CAS  Google Scholar 

  46. 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 100:245–257

    Article  PubMed  Google Scholar 

  47. Cleary DFR, de Voogd NJ, Polónia ARM, Freitas R, Gomes NC (2015) Composition and predictive functional analysis of bacterial communities in seawater, sediment and sponges in the Spermonde Archipelago, Indonesia. Microb. Ecol. 70:889–903

    Article  PubMed  CAS  Google Scholar 

  48. 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:fiv019. https://doi.org/10.1093/femsec/fiv019

    Article  PubMed  CAS  Google Scholar 

  49. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  PubMed  CAS  Google Scholar 

  51. Edgar R, Haas B, Clemente J, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Wang Q, Garrity G, Tiedje J, Cole J (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73:5261–5267. https://doi.org/10.1128/AEM.00062-07

    Article  CAS  Google Scholar 

  53. 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/

    Google Scholar 

  54. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7:203–214. https://doi.org/10.1089/10665270050081478

    Article  PubMed  CAS  Google Scholar 

  55. 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. https://doi.org/10.1038/nbt.2676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. 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. https://doi.org/10.1007/s00248-013-0365-2

    Article  Google Scholar 

  57. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2:4–3 https://CRAN.R-project.org/package=vegan

    Google Scholar 

  58. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. https://doi.org/10.1007/s004420100716

    Article  PubMed  Google Scholar 

  59. Cleary DFR (2003) An examination of scale of assessment, logging and ENSO-induced fires on butterfly diversity in Borneo. Oecologia 135:313–321. https://doi.org/10.1007/s00442-003-1188-5

    Article  PubMed  Google Scholar 

  60. Coelho FJRC, Louvado A, Domingues P, Cleary DFR, Ferreira M, Almeida A, Cunha MR, Cunha Â, Gomes NCM (2016) Integrated characterization of bacterial and microeukaryotic communities in non-active to active mud volcanoes in the Gulf of Cadiz. Sci. Rep. 6:35272. https://doi.org/10.1038/srep35272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Coelho FJRC, Cleary DFR, Rocha RJM, Calado R, Castanheira J, Silva AMS, Simões MMQ, Oliveira V, Lillebo A, Almeida A, Cunha Â, Lopes I, Ribeiro R, Moreira-Santos M, Marques CR, Costa R, Pereira R, Gomes NCM (2015) Unravelling the interactive effects of climate change and oil contamination on lab-simulated estuarine benthic communities. Glob Change Biol 21:1871–1886. https://doi.org/10.1111/gcb.12801

    Article  Google Scholar 

  62. Stackebrandt E, Rainey FA, Ward-Rainey N (2012) Order I. Acidimicrobiales. In: Whitman W, Goodfellow M, Kämpfer P, Hans-Jürgen B, Trujillo M, Ludwig W et al (eds) Bergey’s manual of systematic bacteriology: volume 5: the Actinobacteria. Springer, New York, p 1750

    Google Scholar 

  63. Monier A, Findlay HS, Charvet S, Lovejoy C (2014) Late winter under ice pelagic microbial communities in the high Arctic Ocean and the impact of short-term exposure to elevated CO2 levels. Front. Microbiol. 5:490. https://doi.org/10.3389/fmicb.2014.00490

    Article  PubMed  PubMed Central  Google Scholar 

  64. Taylor JD, Ellis R, Milazzo M, Hall-Spencer JM, Cunliffe M (2014) Intertidal epilithic bacteria diversity changes along a naturally occurring carbon dioxide and pH gradient. FEMS Microbiol. Ecol. 89:670–678. https://doi.org/10.1111/1574-6941.12368

    Article  PubMed  CAS  Google Scholar 

  65. Webster NS, Negri AP, Botté ES, Laffy PW, Flores F, Noonan S, Schmidt C, Uthicke S (2016) Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6:19324. https://doi.org/10.1038/srep19324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Fu FX, Warner ME, Zhang YH, Feng YY, Hutchins DA (2007) Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J. Phycol. 43:485–496. https://doi.org/10.1111/j.1529-8817.2007.00355.x

    Article  Google Scholar 

  67. Xia X, Guo W, Tan S, Liu H (2017) Synechococcus assemblages across the salinity gradient in a salt wedge estuary. Front. Microbiol. 8:1254. https://doi.org/10.3389/fmicb.2017.01254. ECollection 2017

  68. Liu X, Xiao WP, Landry MR, Chiang KP, Wang L, Huang BQ (2016) Responses of phytoplankton communities to environmental variability in the East China Sea. Ecosystems 19:832–849

    Article  CAS  Google Scholar 

  69. Cho JC, Giovannoni SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl. Environ. Microbiol. 70:432–440. https://doi.org/10.1128/aem.70.1.432-440.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Morrow KM, Bourne DG, Humphrey C, Botté ES, Laffy P, Zaneveld J, Uthicke S, Fabricius KE, Webster NS (2015) Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. ISME J 9:894–908. https://doi.org/10.1038/ismej.2014.188

    Article  PubMed  CAS  Google Scholar 

  71. Ribes M, Calvo E, Movilla J, Logares R, Coma R, Pelejero C (2016) Restructuring of the sponge microbiome favors tolerance to ocean acidification. Environ. Microbiol. Rep. 8:536–544. https://doi.org/10.1111/1758-2229.12430

    Article  PubMed  CAS  Google Scholar 

  72. Cleary DFR, Polónia ARM, Becking LE, de Voogd NJ, Purwanto GH, Gomes NCM (2017) Compositional analysis of bacterial communities in seawater, sediment and high and low microbial abundance sponges in the Misool coral reef system, Indonesia. Mar. Biodivers.:1–13. https://doi.org/10.1007/s12526-017-0697-0

  73. Innocenti F (ed) (2008) Genomics and pharmacogenomics in anticancer drug development and clinical response. Humana Press, New York, USA, p 378. https://doi.org/10.1007/978-1-60327-088-5

    Book  Google Scholar 

  74. Eggleston AK (2007) DNA replication and repair. Nature 447:923–923. https://doi.org/10.1038/447923a

    Article  CAS  Google Scholar 

  75. Shigenobu S, Watanabe H, Hattori M, SaKi Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86. https://doi.org/10.1038/35024074

    Article  PubMed  CAS  Google Scholar 

  76. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, Aksoy S (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402–407. https://doi.org/10.1038/ng986

    Article  PubMed  CAS  Google Scholar 

  77. Dale C, Wang B, Moran N, Ochman H (2003) Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol 20:1188–1194. https://doi.org/10.1093/molbev/msg138

    Article  PubMed  CAS  Google Scholar 

  78. Pompella A, Visvikis A, Paolicchi A, De Tata V, Casini AF (2003) The changing faces of glutathione, a cellular protagonist. Biochem. Pharmacol. 66:1499–1503. https://doi.org/10.1016/S0006-2952(03)00504-5

    Article  PubMed  CAS  Google Scholar 

  79. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot. 76:16–179. https://doi.org/10.1016/j.sajb.2009.10.007

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to the Indonesian State Ministry of Research and Technology (RISTEK) for providing research permits. We thank the following people for their help in various ways: Leontine Becking, Rossana Freitas, Suharsono, Y. Tuti, E.Oberhauser, R. Suhr and the staff of Nabucco Island Dive Resort.

Funding

The research was sponsored by the Indonesian Institute of Sciences (LIPI) and funded by the Portuguese Foundation for Science and Technology, FCT, project LESS CORAL, PTDC/AAC-AMB/115304/2009. Ana R.M. Polónia was supported by a postdoctoral scholarship [SFRH/BPD/117563/2016] funded by FCT, Portugal (QREN-POPH Type 4.1—Advanced Training, subsidised by the European Social Fund and national funds MCTES). Thanks are also due, for the financial support to CESAM [UID/AMB/50017], to FCT/MEC through national funds and co-funding by FEDER, within the PT2020 Partnership Agreement and Compete 2020.

Author information

Authors and Affiliations

  1. Department of Biology, CESAM, Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Daniel F. R. Cleary & Ana R. M. Polónia

  2. Naturalis Biodiversity Center, 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. Ana R. M. Polónia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicole J. de Voogd
    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

ESM 1

(XLS 9 kb)

ESM 2

(R 32 kb)

ESM 3

(CSV 1615 kb)

ESM 4

(PDF 9 kb)

ESM 5

(PDF 9 kb)

ESM 6

(DOC 13 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., Polónia, A.R.M. & de Voogd, N.J. Bacterial Communities Inhabiting the Sponge Biemna fortis, Sediment and Water in Marine Lakes and the Open Sea. Microb Ecol 76, 610–624 (2018). https://doi.org/10.1007/s00248-018-1156-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1156-6

Keywords

Search

Navigation