Skip to main content

Advertisement

Log in

Variations in Microbial Diversity and Metabolite Profiles of the Tropical Marine Sponge Xestospongia muta with Season and Depth

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Xestospongia muta is among the most emblematic sponge species inhabiting coral reefs of the Caribbean Sea. Besides being the largest sponge species growing in the Caribbean, it is also known to produce secondary metabolites. This study aimed to assess the effect of depth and season on the symbiotic bacterial dynamics and major metabolite profiles of specimens of X. muta thriving in a tropical marine biome (Portobelo Bay, Panamá), which allow us to determine whether variability patterns are similar to those reported for subtropical latitudes. The bacterial assemblages were characterized using Illumina deep-sequencing and metabolomic profiles using UHPLC-DAD-ELSD from five depths (ranging 9–28 m) across two seasons (spring and autumn). Diverse symbiotic communities, representing 24 phyla with a predominance of Proteobacteria and Chloroflexi, were found. Although several thousands of OTUs were determined, most of them belong to the rare biosphere and only 23 to a core community. There was a significant difference between the structure of the microbial communities in respect to season (autumn to spring), with a further significant difference between depths only in autumn. This was partially mirrored in the metabolome profile, where the overall metabolite composition did not differ between seasons, but a significant depth gradient was observed in autumn. At the phyla level, Cyanobacteria, Firmicutes, Actinobacteria, and Spirochaete showed a mild-moderate correlation with the metabolome profile. The metabolomic profiles were mainly characterized by known brominated polyunsaturated fatty acids. This work presents findings about the composition and dynamics of the microbial assemblages of X. muta expanding and confirming current knowledge about its remarkable diversity and geographic variability as observed in this tropical marine biome.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Li CW, Chen JY, Hua TE (1998) Precambrian sponges with cellular structures. Science 279:879–882. https://doi.org/10.1126/science.279.5352.879

    Article  CAS  PubMed  Google Scholar 

  2. Yin Z, Zhu M, Davidson EH, Bottjer DJ, Zhao F, Tafforeau P (2015) Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci U S A 112:E1453–E1460. https://doi.org/10.1073/pnas.1414577112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Van-Soest R, Boury-Esnault N, Vacelet J et al (2012) Global diversity of sponges (Porifera). PLoS One 7:e35105. https://doi.org/10.1371/journal.pone.0035105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Gold DA, Grabenstatter J, De Mendoza A et al (2016) Sterol and genomic analyses validate the sponge biomarker hypothesis. Proc Natl Acad Sci 1–6:2684–2689. https://doi.org/10.1073/pnas.1512614113

    Article  CAS  Google Scholar 

  5. Dayton PK (1989) Interdecadal variation in an antarctic sponge and its predators from oceanographic climate shifts. Science 245:1484–1486. https://doi.org/10.1126/science.245.4925.1484

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  PubMed  Google Scholar 

  7. 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

    Article  Google Scholar 

  8. Deignan LK, Pawlik JR (2014) Perilous proximity: does the Janzen-Connell hypothesis explain the distribution of giant barrel sponges on a Florida coral reef? Coral Reefs 34:561–567. https://doi.org/10.1007/s00338-014-1255-x

    Article  Google Scholar 

  9. Rix L, Naumann MS, de Goeij JM et al (2015) Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems. Scientific 6:1–11. https://doi.org/10.1038/srep18715

    Article  CAS  Google Scholar 

  10. Pawlik JR, McMurray SE, Erwin P, Zea S (2015) No evidence for food limitation of Caribbean reef sponges: reply to Slattery & Lesser (2015). Mar Ecol Prog Ser 527:281–284. https://doi.org/10.3354/meps11308

    Article  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. Loh T-L, Pawlik JR (2014) Chemical defenses and resource trade-offs structure sponge communities on Caribbean coral reefs. Proc Natl Acad Sci U S A 111:4151–4156. https://doi.org/10.1073/pnas.1321626111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhang F, Blasiak LC, Karolin JO, Powell RJ, Geddes CD, Hill RT (2015) Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. Proc Natl Acad Sci 201423768:4381–4386. https://doi.org/10.1073/pnas.1423768112

    Article  CAS  Google Scholar 

  14. Gatti S (2002) The role of sponges in high-Antarctic carbon and silicon cycling—a modelling approach. Ber Polarforsch Meeresforsch 434:1–134

    Google Scholar 

  15. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Indraningrat AAG, Smidt H, Sipkema D (2016) Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar Drugs 14:1–66. https://doi.org/10.3390/md14050087

    Article  CAS  Google Scholar 

  17. Li Z-Y, He L-M, Wu J, Jiang Q (2006) Bacterial community diversity associated with four marine sponges from the South China Sea based on 16S rDNA-DGGE fingerprinting. J Exp Mar Biol Ecol 329:75–85. https://doi.org/10.1016/j.jembe.2005.08.014

    Article  CAS  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346. https://doi.org/10.1111/j.1462-2920.2011.02460.x

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. Vacelet J, Donadey C (1975) Electron microscope study of the association between some sponges and bacteria. Bio Ecol 30:301–314

    Article  Google Scholar 

  22. Webster NS, Thomas T (2016). Defining the Sponge Hologenome 7:1–14. https://doi.org/10.1128/mBio.00135-16.Invited

    Article  Google Scholar 

  23. Ribes M, Jiménez E, Yahel G, López-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. https://doi.org/10.1111/j.1462-2920.2012.02701.x

    Article  CAS  PubMed  Google Scholar 

  24. Thoms C, Schupp P (2007) Chemical defense strategies in sponges: a review. Porifera Res Biodiversity Innov Sustain 627–637

  25. Leal MC, Puga J, Serôdio J, Gomes NCM, Calado R (2012) Trends in the discovery of new marine natural products from invertebrates over the last two decades—where and what are we bioprospecting? PLoS One 7:e30580. https://doi.org/10.1371/journal.pone.0030580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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  CAS  PubMed  Google Scholar 

  27. 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  CAS  Google Scholar 

  28. Morinaka BI, Skepper CK, Molinski TF (2007) Ene-yne tetrahydrofurans from the sponge Xestospongia muta. Exploiting a Weak CD Effect for Assignment of Configuration 1:3–6

    Google Scholar 

  29. Schmitz FJ, Gopichand Y (1978) (7E,13E,15Z)-14,16-dibromo-7,13,15-hexadecatrien-5-ynoic acid. A novel dibromo acetylenic acid from the marine sponge Xestospongia muta. Tetrahedron Lett 3637–3640

  30. 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. https://doi.org/10.1016/j.chemphyslip.2011.08.002

    Article  CAS  PubMed  Google Scholar 

  31. McMurray SE, Finelli CM, Pawlik JR (2015) Population dynamics of giant barrel sponges on Florida coral reefs. J Exp Mar Biol Ecol 473:73–80. https://doi.org/10.1016/j.jembe.2015.08.007

    Article  Google Scholar 

  32. Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Schupp P, Pawlik JR, Lindquist NL, Erpenbeck D, Wörheide G, Hentschel U (2014) The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull 227:78–88

    Article  PubMed  Google Scholar 

  33. Zhou X, Xu T, Yang X-W, Huang R, Yang B, Tang L, Liu Y (2010) Chemical and biological aspects of marine sponges of the genus Xestospongia. Chem Biodivers 7:2201–2227. https://doi.org/10.1002/cbdv.201000024

    Article  CAS  PubMed  Google Scholar 

  34. Giannini A, Kushnir Y, Cane MA (2000) Interannual variability of Caribbean rainfall, ENSO, and the Atlantic Ocean. J Clim 13:297–311. https://doi.org/10.1175/1520-0442(2000)013<0297:IVOCRE>2.0.CO;2

    Article  Google Scholar 

  35. 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 155:159–171. https://doi.org/10.1007/s00227-008-1014-z

    Article  Google Scholar 

  36. Griffiths R, Whiteley A (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA-and rRNA-based microbial community composition. Appl Environ Microbiol 66:1–5. https://doi.org/10.1128/AEM.66.12.5488-5491.2000.Updated

    Article  Google Scholar 

  37. Simister RL, Schmitt S, Taylor MW (2011) Evaluating methods for the preservation and extraction of DNA and RNA for analysis of microbial communities in marine sponges. J Exp Mar Biol Ecol 397:38–43. https://doi.org/10.1016/j.jembe.2010.11.004

    Article  CAS  Google Scholar 

  38. Bohorquez LC, Delgado-Serrano L, López G, Osorio-Forero C, Klepac-Ceraj V, Kolter R, Junca H, Baena S, Zambrano MM (2012) In-depth characterization via complementing culture-independent approaches of the microbial community in an acidic hot spring of the Colombian Andes. Microb Ecol 63:103–115. https://doi.org/10.1007/s00248-011-9943-3

    Article  PubMed  Google Scholar 

  39. Galvez E, Junca H, Riaño D (2012) Assessment of microbial composition and degradation functions in PAH contaminated neotropical Caribbean marine sediments (Cartagena Bay, Colombia). Universidad de Los Andes

  40. Camarinha-Silva A, Juregui R, Chaves-Moreno D et al (2014) Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ Microbiol 16:2939–2952. https://doi.org/10.1111/1462-2920.12362

    Article  CAS  PubMed  Google Scholar 

  41. Kuczynski J, Stombaugh J, Walters WA et al (2011) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Bioinformatics Chapter 10:Unit 10.7. https://doi.org/10.1002/0471250953.bi1007s36

    Article  Google Scholar 

  42. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. https://doi.org/10.1093/bioinformatics/btp636

    Article  CAS  PubMed  Google Scholar 

  43. Ivanišević J, Thomas OP, Lejeusne C, Chevaldonné P, Pérez T (2010) 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

    Article  CAS  Google Scholar 

  44. Greff S, Zubia M, Payri C, Thomas OP, Perez T (2017) Chemogeography of the red macroalgae Asparagopsis: metabolomics, bioactivity, and relation to invasiveness. Metabolomics 13:0. https://doi.org/10.1007/s11306-017-1169-z

    Article  CAS  Google Scholar 

  45. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27. https://doi.org/10.1038/ismej.2009.97

    Article  CAS  PubMed  Google Scholar 

  46. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edition. Prim Plymouth UK p. 172

  47. Anderson MJ (2001) A new method for non parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x

    Article  Google Scholar 

  48. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Hollister EB, Engledow AS, Hammett AJM, Provin TL, Wilkinson HH, Gentry TJ (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838. https://doi.org/10.1038/ismej.2010.3

    Article  CAS  PubMed  Google Scholar 

  50. Barberan A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. Isme J 6:343–351. https://doi.org/10.1038/ismej.2011.119

    Article  CAS  PubMed  Google Scholar 

  51. Fiore CL, Jarett JK, Lesser MP (2013) Symbiotic prokaryotic communities from different populations of the giant barrel sponge, Xestospongia muta. Microbiologyopen 2:938–952. https://doi.org/10.1002/mbo3.135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 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. https://doi.org/10.1128/AEM.05285-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB, Erwin PM, López-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870. https://doi.org/10.1038/ncomms11870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S, Horn M, Wagner M (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. 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 (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576. https://doi.org/10.1038/ismej.2011.116

    Article  CAS  PubMed  Google Scholar 

  56. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW (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

    Article  CAS  PubMed  Google Scholar 

  57. Patil A, Kokke W, Cochran S et al (1992) Brominated polyacetylenic acids from the marine sponge Xestospongia muta: inhibitors of HIV protease. J Nat Prod 55:1170–1177

    Article  CAS  PubMed  Google Scholar 

  58. Morrow KM, Fiore C, Lesser M (2016) Environmental drivers of microbial community shifts in the giant barrel sponge, Xestospongia muta, over a shallow to mesophotic depth gradient. Environ Microbiol n/a-n/a. https://doi.org/10.1111/1462-2920.13226

  59. Olson JB, Gao X (2013) Characterizing the bacterial associates of three Caribbean sponges along a gradient from shallow to mesophotic depths. FEMS Microbiol Ecol 85:74–84. https://doi.org/10.1111/1574-6941.12099

    Article  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. Appl Environ Microbiol 74:7694–7708. https://doi.org/10.1128/AEM.00878-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lesser MP, Fiore C, Slattery M, Zaneveld J (2016) Climate change stressors destabilize the microbiome of the Caribbean barrel sponge, Xestospongia muta. J Exp Mar Biol Ecol 475:11–18. https://doi.org/10.1016/j.jembe.2015.11.004

    Article  Google Scholar 

  62. Wilkinson C (1978) Microbial associations in sponges. III. Ultrastructure of the in situ associations in coral reef sponges. Mar Biol 49:177–185

    Article  Google Scholar 

  63. Burgsdorf I, Slaby BM, Handley KM, Haber M, Blom J, Marshall CW, Gilbert JA, Hentschel U, Steindler L (2015) Lifestyle evolution in cyanobacterial symbionts of sponges. MBio 6:1–14. https://doi.org/10.1128/mBio.00391-15

    Article  CAS  Google Scholar 

  64. Usher KM (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar Ecol 29:178–192. https://doi.org/10.1111/j.1439-0485.2008.00245.x

    Article  Google Scholar 

  65. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Preston CM, Wu KY, Molinskit TF, Delong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge. Proc Natl Acad Sci U S A 93:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M, Taylor MW (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10:1087–1094. https://doi.org/10.1111/j.1462-2920.2007.01515.x

    Article  CAS  PubMed  Google Scholar 

  68. Zhang H, Sekiguchi Y, Hanada S et al (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163. https://doi.org/10.1099/ijs.0.02520-0

    Article  CAS  PubMed  Google Scholar 

  69. Lesser MP (2006) Benthic–pelagic coupling on coral reefs: feeding and growth of Caribbean sponges. J Exp Mar Biol Ecol 328:277–288. https://doi.org/10.1016/j.jembe.2005.07.010

    Article  Google Scholar 

  70. 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

    Article  CAS  Google Scholar 

  71. Kennedy J, Baker P, Piper C, Cotter PD, Walsh M, Mooij MJ, Bourke MB, Rea MC, O’Connor PM, Ross RP, Hill C, O’Gara F, Marchesi JR, Dobson ADW (2009) Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar Biotechnol 11:384–396. https://doi.org/10.1007/s10126-008-9154-1

    Article  CAS  Google Scholar 

  72. Fiore CL, Labrie M, Jarett JK, Lesser MP (2015) Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: molecular evidence for metabolic interchange. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00364, 6

Download references

Acknowledgments

We thank the additional support from Dr. Regis Guillaume, Embassy of France in Colombia, and Raúl de León from Dive Adventure Panama and Portobelo Dive Center for his guidance and collaboration during the dive sampling, to Iris Plumeier and Silke Kahl for excellent technical assistance and to the members of the BIOMMAR research group for their helpful technical advices.

Funding

The authors would like to thank financial support granted by the European Commission to EC/FP7 research project consortium MAGICPAH (KBBE-2009-245226), to the Colombian Administrative Department for Science, Technology and Innovation - Colciencias for financial support through grants EcosNord-Colciencias (Convocatoria 652-2014) “International cooperation and research mobility grants in marine research between Colombia and France 2015-2017” and “Joven Investigador” 2012 fellowship to M. Villegas-Plazas and to Universidad de los Andes for the MSc scholarship to M. Villegas-Plazas.

Author information

Authors and Affiliations

Authors

Contributions

MV analyzed and interpreted the microbial community data and wrote the manuscript. OT analyzed and interpreted the metabolomic data. MO supported statistical analyses. HJ conceptualized, analyzed the results, and supervised the study. JS contributed with the experimental design and DP with the sequencing and analyzing the results. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Howard Junca.

Ethics declarations

Ethics Approval and Consent to Participate

Not applicable

Consent for Publication

Not applicable

Competing Interests

The authors declare that they have no competing interests.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Villegas-Plazas, M., Wos-Oxley, M.L., Sanchez, J.A. et al. Variations in Microbial Diversity and Metabolite Profiles of the Tropical Marine Sponge Xestospongia muta with Season and Depth. Microb Ecol 78, 243–256 (2019). https://doi.org/10.1007/s00248-018-1285-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1285-y

Keywords

Navigation