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Genus-specific associations of marine sponges with group I crenarchaeotes

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Abstract

Sponges have rich and diverse associated microbial communities, which may have important functions in their metabolism. A survey of the archaeal communities of 23 poriferan species, focusing on the family Axinellidae, was conducted over the period 2002–2004 using 16S rDNA gene libraries created with archaeal-specific primers. The 28S rDNA sequences of the sponge hosts were also obtained. Of 23 species, 19 showed evidence of archaeal communities from group C1a (marine group I; Crenarchaeota), with three of these also showing evidence of Archaea from group E2 (marine group II; Euryarchaeota). Within the Crenarchaeota, two strongly supported sponge-specific clades were identified corresponding to the sponge family Axinellidae, and a novel sponge clade denoted clade C. These findings suggest that these archaea have evolved closely with their sponge hosts and are likely to play an important role in their metabolism.

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Notes

  1. In the original article, these groups were designated marine groups I and II. Designation was changed to agree with that used by DeLong and Pace (2001).

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Alvarez B, Crisp MD, Driver F, Hooper JNA, Van Soest RWM (2000) Phylogenetic relationships of the family Axinellidae (Porifera: Demospongiae) using morphological and molecular data. Zool Scr 29:169–198

    Article  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucleic Acids Res 33:D34–D38

    Article  CAS  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM, Tiedje JM (2003) The ribosomal database project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson SC, Pace NR (2002) Novel kingdom-level eukaryotic diversity in anoxic environments. PNAS 99:8324-8329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeLong E (1992) Archaea in coastal marine environments. Proc Natl Acad Sci 89:5685–5689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50:470–478

    Article  CAS  PubMed  Google Scholar 

  • Dojka MA, Hugenholtz P, Haack SK, Pace NR (1998) Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl Environ Microbiol 64:3869–3877

    CAS  PubMed  PubMed Central  Google Scholar 

  • Erpenbeck D, Breeuwer JAJ, Soest RWM (2005) Implications from a 28S rRNA gene fragment for the phylogenetic relationships of halichondrid sponges (Porifera: Demospongiae). J Zool Syst Evol 43:93–99

    Article  Google Scholar 

  • Faulkner DJ (2000) Marine natural products. Nat Prod Rep 17:5–55

    Google Scholar 

  • Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum “poribacteria” in marine sponges. Appl Environ Microbiol 70:3724–3732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356:148–149

    Article  CAS  PubMed  Google Scholar 

  • Hassouna N, Michot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirabayashi J, Kasai K (1993) The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function, and molecular evolution. Glycobiology 3:297–304

    Article  CAS  PubMed  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol 3:1–8

    Article  Google Scholar 

  • Lee EY, Lee HK, Lee YK, Sim CJ, Lee JH (2003) Diversity of symbiotic archaeal communities in marine sponges from Korea. Biomol Eng 20:299–304

    Article  CAS  PubMed  Google Scholar 

  • Ludwig W (2001) LSU rRNA ARB database. Available at http://www2.mikro.biologie.tu-muenchen.de /download/ ARB/data/3pubmrz99.arb

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margot H, Acebal C, Toril E, Amils R, Puentes JLF (2002) Consistent association of crenarchaeal Archaea with sponges of the genus Axinella. Mar Biol 140:739–745

    Article  CAS  Google Scholar 

  • Massana R, Murray A, Preston C, DeLong E (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63:50–56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Munro MHG, Blunt JW, Dumdei EJ, Hickford SJH, Lill RE, Li S, Battershill CN, Duckworth AR (1999) The discovery and development of marine compounds with pharmaceutical potential. J Biotechnol 70:15–25

    Article  CAS  PubMed  Google Scholar 

  • Nichols SA (2005) An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Mol Phylogenet Evol 34:81–96

    Article  CAS  PubMed  Google Scholar 

  • Osinga R, Armstrong E, Burgess JG, Hoffmann F, Reitner J, Schumann-Kindel G (2001) Sponge-microbe associations and their importance for sponge bioprocess engineering. Hydrobiologia 461:55–62

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • 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 93:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Huelsenbeck JP, van der Mark P (2005) MrBayes 3.1 Manual. School of Computational Science, Florida State University

  • Schleper C, DeLong EF, Preston CM, Feldman RA, Wu KY, Swanson RV (1998) Genomic analysis reveals chromosomal variation in natural populations of the uncultured psychrophilic archaeon Cenarchaeum symbiosum. J Bacteriol 180:5003–5009

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488

    Article  CAS  PubMed  Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer-Verlag, New York

    Book  Google Scholar 

  • Sipkema D, van Wielink R, van Lammeren AA, Tramper J, Osinga R, Wijffels RH (2003) Primmorphs from seven marine sponges: formation and structure. J Biotechnol 100:127–139

    Article  CAS  PubMed  Google Scholar 

  • Stahl DA, Amann RI (1991) Development and applicaiton of nucleic acid probes in bacterial systematics. Sequencing and hybridization techniques in bacterial systematics. Wiley, London, pp 205–248

    Google Scholar 

  • Swofford DL (2003) Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MA

  • Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Microbiol Ecol 30:301–314

    Article  Google Scholar 

  • Webster NS, Watts JEM, Hill RT (2001) Detection and phylogenetic analysis of novel crenarchaeote and euryarchaeote 16S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotechnol 3:600–608

    Article  CAS  Google Scholar 

  • Webster NS, Negri AP, Munro MM, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the National Science Foundation under Award Number EEC-9731725 and BES-0337080. We would like to acknowledge: Dr. Belinda Alvarez de Glasby of The Museum and Art Gallery of the Northern Territory for providing and identifying many of the axinellid sponges used in this study, Christina Preston of MBARI for DNA samples and her suggestions for the direction of this project, and Scott Nichols for providing DNA samples, technical advice, discussions, and comments on earlier drafts of this manuscript. We also thank Gilbert Basbas Jr., Nathan Cheng, Bernadette Cortes, and Katherine Wang for their assistance in conducting parts of the experimental studies.

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  1. Department of Chemical Engineering, University of California, Berkeley, CA, 94720, USA

    Bradley Holmes & Harvey Blanch

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  1. Bradley Holmes
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  2. Harvey Blanch
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Correspondence to Bradley Holmes.

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Communicated by J.P. Grassle, New Brunswick

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

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