Skip to main content

Advertisement

SpringerLink
Log in

Pyrosequencing Reveals the Microbial Communities in the Red Sea Sponge Carteriospongia foliascens and Their Impressive Shifts in Abnormal Tissues

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

Abstract

Abnormality and disease in sponges have been widely reported, yet how sponge-associated microbes respond correspondingly remains inconclusive. Here, individuals of the sponge Carteriospongia foliascens under abnormal status were collected from the Rabigh Bay along the Red Sea coast. Microbial communities in both healthy and abnormal sponge tissues and adjacent seawater were compared to check the influences of these abnormalities on sponge-associated microbes. In healthy tissues, we revealed low microbial diversity with less than 100 operational taxonomic units (OTUs) per sample. Cyanobacteria, affiliated mainly with the sponge-specific species “Candidatus Synechococcus spongiarum,” were the dominant bacteria, followed by Bacteroidetes and Proteobacteria. Intraspecies dynamics of microbial communities in healthy tissues were observed among sponge individuals, and potential anoxygenic phototrophic bacteria were found. In comparison with healthy tissues and the adjacent seawater, abnormal tissues showed dramatic increase in microbial diversity and decrease in the abundance of sponge-specific microbial clusters. The dominated cyanobacterial species Candidatus Synechococcus spongiarum decreased and shifted to unspecific cyanobacterial clades. OTUs that showed high similarity to sequences derived from diseased corals, such as Leptolyngbya sp., were found to be abundant in abnormal tissues. Heterotrophic Planctomycetes were also specifically enriched in abnormal tissues. Overall, we revealed the microbial communities of the cyanobacteria-rich sponge, C. foliascens, and their impressive shifts under abnormality.

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. Hedges SB, Blair JE, Venturi ML, Shoe JL (2004) A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 4:2. doi:10.1186/1471-2148-4-2

    Article  PubMed Central  PubMed  Google Scholar 

  2. Vogel G (2008) The inner lives of sponges. Science 320:1028–1030. doi:10.1126/science.320.5879.1028

    Article  CAS  PubMed  Google Scholar 

  3. Vacelet J, Donadey C (1977) Electron-microscope study of association between some sponges and bacteria. J Exp Mar Bio Ecol 30:301–314. doi:10.1016/0022-0981(77)90038-7

    Article  Google Scholar 

  4. Lee OO, Wang Y, Yang JK, 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 

  5. 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. doi:10.1038/ismej.2011.116

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  7. Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9:1363–1375. doi:10.1111/j.1462-2920.2007.01303.x

    Article  CAS  PubMed  Google Scholar 

  8. Webster NS, Negri AP, Webb RI, Hill RT (2002) A spongin-boring alpha-proteobacterium is the etiological agent of disease in the Great Barrier Reef sponge Rhopaloeides odorabile. Mar Ecol Prog Ser 232:305–309. doi:10.3354/Meps232305

    Article  Google Scholar 

  9. Erwin PM, Pita L, Lopez-Legentil S, Turon X (2012) Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl Environ Microbiol 78:7358–7368. doi:10.1128/Aem.02035-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Wang Y, Qian PY (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4:e7401. doi:10.1371/journal.pone.0007401

    Article  PubMed Central  PubMed  Google Scholar 

  11. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Moller K (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68:673–690. doi:10.1128/AEM.68.2.673-690.2002

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/Nmeth.F.303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669. doi:10.1038/nmeth0910-668b

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  15. 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. doi:10.1093/bioinformatics/btp636

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi:10.1093/nar/gkm864

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, Petrosino JF, Knight R, Birren BW, Consortium HM (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. doi:10.1101/gr.112730.110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/AEM.00062-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454. doi:10.1093/bioinformatics/bth078

    Article  PubMed  Google Scholar 

  20. Simister R, Taylor MW, Tsai P, Fan L, Bruxner TJ, Crowe ML, Webster N (2012) Thermal stress responses in the bacterial biosphere of the Great Barrier Reef sponge, Rhopaloeides odorabile. Environ Microbiol 14:3232–3246. doi:10.1111/1462-2920.12010

    Article  CAS  PubMed  Google Scholar 

  21. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/Nar/Gkh340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Myers JL, Sekar R, Richardson LL (2007) Molecular detection and ecological significance of the cyanobacterial genera Geitlerinema and Leptolyngbya in black band disease of corals. Appl Environ Microbiol 73:5173–5182. doi:10.1128/AEM.00900-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Binladen J, Gilbert MT, Bollback JP, Panitz F, Bendixen C, Nielsen R, Willerslev E (2007) The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One 2:e197. doi:10.1371/journal.pone.0000197

    Article  PubMed Central  PubMed  Google Scholar 

  24. Zhou J, Wu L, Deng Y, Zhi X, Jiang YH, Tu Q, Xie J, Van Nostrand JD, He Z, Yang Y (2011) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5:1303–1313. doi:10.1038/ismej.2011.11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Pinto AJ, Raskin L (2012) PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS One 7:e43093. doi:10.1371/journal.pone.0043093

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Lemos LN, Fulthorpe RR, Roesch LF (2012) Low sequencing efforts bias analyses of shared taxa in microbial communities. Folia Microbiol (Praha) 57:409–413. doi:10.1007/s12223-012-0155-0

    Article  CAS  Google Scholar 

  27. Lemloh ML, Fromont J, Brummer F, Usher KM (2009) Diversity and abundance of photosynthetic sponges in temperate Western Australia. BMC Ecol 9:4. doi:10.1186/1472-6785-9-4

    Article  PubMed Central  PubMed  Google Scholar 

  28. White JR, Patel J, Ottesen A, Arce G, Blackwelder P, Lopez JV (2012) Pyrosequencing of bacterial symbionts within Axinella corrugata sponges: diversity and seasonal variability. PLoS One 7:e38204. doi:10.1371/journal.pone.0038204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH (2013) Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31:533–538. doi:10.1038/nbt.2579

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496. doi:10.1016/j.tim.2006.09.001

    Article  CAS  PubMed  Google Scholar 

  32. Imhoff JF, Trüper HG (1976) Marine sponges as habitats of anaerobic phototrophic bacteria. Microb Ecol 3:1–9

    Article  CAS  PubMed  Google Scholar 

  33. Imhoff JF (2001) True marine and halophilic anoxygenic phototrophic bacteria. Arch Microbiol 176:243–254. doi:10.1007/s002030100326

    Article  CAS  PubMed  Google Scholar 

  34. Thacker RW (2005) Impacts of shading on sponge-Cyanobacteria symbioses: a comparison between host-specific and generalist associations. Integr Comp Biol 45:369–376. doi:10.1093/Icb/45.2.369

    Article  PubMed  Google Scholar 

  35. Cebrian E, Uriz MJ, Garrabou J, Ballesteros E (2011) Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off? PLoS One 6:e20211. doi:10.1371/journal.pone.0020211

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Angermeier H, Glockner V, Pawlik JR, Lindquist NL, Hentschel U (2012) Sponge white patch disease affecting the Caribbean sponge Amphimedon compressa. Dis Aquat Organ 99:95–102. doi:10.3354/dao02460

    Article  CAS  PubMed  Google Scholar 

  37. Moitinho-Silva L, Bayer K, Cannistraci CV, Giles EC, Ryu T, Seridi L, Ravasi T (2014) 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

    Article  CAS  PubMed  Google Scholar 

  38. Cleary DF, Becking LE, de Voogd NJ, Renema W, de Beer M, van Soest RW, 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. doi:10.1016/j.ecss.2005.06.025

    Article  Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

  40. Dominguez-Escobar J, Beltran Y, Bergman B, Diez B, Ininbergs K, Souza V, Falcon LI (2011) Phylogenetic and molecular clock inferences of cyanobacterial strains within Rivulariaceae from distant environments. Fems Microbiol Lett 316:90–99. doi:10.1111/j.1574-6968.2010.02195.x

    Article  CAS  PubMed  Google Scholar 

  41. Sihvonen LM, Lyra C, Fewer DP, Rajaniemi-Wacklin P, Lehtimaki JM, Wahlsten M, Sivonen K (2007) Strains of the cyanobacterial genera Calothrix and Rivularia isolated from the Baltic Sea display cryptic diversity and are distantly related to Gloeotrichia and Tolypothrix. FEMS Microbiol Ecol 61:74–84. doi:10.1111/j.1574-6941.2007.00321.x

    Article  CAS  PubMed  Google Scholar 

  42. Angermeier H, Kamke J, Abdelmohsen UR, Krohne G, Pawlik JR, Lindquist NL, Hentschel U (2011) The pathology of sponge orange band disease affecting the Caribbean barrel sponge Xestospongia muta. FEMS Microbiol Ecol 75:218–230. doi:10.1111/j.1574-6941.2010.01001.x

    Article  CAS  PubMed  Google Scholar 

  43. Webster NS, Xavier JR, Freckelton M, Motti CA, Cobb R (2008) Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ Microbiol 10:3366–3376. doi:10.1111/j.1462-2920.2008.01734.x

    Article  CAS  PubMed  Google Scholar 

  44. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9:403–413. doi:10.1038/Nrmicro2578

    Article  CAS  PubMed  Google Scholar 

  45. Wegner CE, Richter-Heitmann T, Klindworth A, Klockow C, Richter M, Achstetter T, Glockner FO, Harder J (2013) Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula. Mar Genomics 9:51–61. doi:10.1016/j.margen.2012.12.001

    Article  PubMed  Google Scholar 

  46. Kamke J, Sczyrba A, Ivanova N, Schwientek P, Rinke C, Mavromatis K, Woyke T, Hentschel U (2013) Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. ISME J 7:2287–300. doi:10.1038/ismej.2013.111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank WP Zhang and G Zhang from Hong Kong University of Science and Technology (HKUST) and the technical team from King Abdullah University of Science and Technology (KAUST) for technical help during sample collection. The authors also thank Professor Rob von Soest, Zoological Museum, University of Amsterdam, for identification of sponges. This study was supported by a grant (U13012056) from the National Science Foundation of China, a grant from China Ocean Mineral Resource Research and Development Association (COMRRDA12SC02), and an award (SA-C0040/UK-C0016) granted to P.Y. Qian from the King Abdullah University of Science and Technology. FFL is supported by the KAUST Special Collaborative Partnership grant. VBB is supported by the KAUST Base Research Funds.

Author information

Authors and Affiliations

  1. Division of Life Science, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, People’s Republic of China

    Zhao-Ming Gao, Yong Wang, On On Lee, Ren-Mao Tian, Yue Him Wong, Salim Bougouffa & Pei-Yuan Qian

  2. Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration (SOA), Xiamen, 361005, People’s Republic of China

    Zhao-Ming Gao

  3. Sanya Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Hai Nan, People’s Republic of China

    Zhao-Ming Gao & Yong Wang

  4. Coastal and Marine Resources Core Lab, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    Zenon Batang & Abdulaziz Al-Suwailem

  5. Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900, Saudi Arabia

    Salim Bougouffa, Feras F. Lafi & Vladimir B. Bajic

Authors
  1. Zhao-Ming Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. On On Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ren-Mao Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yue Him Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Salim Bougouffa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zenon Batang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Abdulaziz Al-Suwailem
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Feras F. Lafi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Vladimir B. Bajic
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Pei-Yuan Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pei-Yuan Qian.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 1212 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, ZM., Wang, Y., Lee, O.O. et al. Pyrosequencing Reveals the Microbial Communities in the Red Sea Sponge Carteriospongia foliascens and Their Impressive Shifts in Abnormal Tissues. Microb Ecol 68, 621–632 (2014). https://doi.org/10.1007/s00248-014-0419-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0419-0

Keywords

Search

Navigation