Skip to main content

Advertisement

Log in

Isolation and diversity of planctomycetes from the sponge Niphates sp., seawater, and sediment of Moreton Bay, Australia

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Planctomycetes are ubiquitous in marine environment and were reported to occur in association with multicellular eukaryotic organisms such as marine macroalgae and invertebrates. Here, we investigate planctomycetes associated with the marine sponge Niphates sp. from the sub-tropical Australian coast by assessing their diversity using culture-dependent and -independent approaches based on the 16S rRNA gene. The culture-dependent approach resulted in the isolation of a large collection of diverse planctomycetes including some novel lineages of Planctomycetes from the sponge as well as sediment and seawater of Moreton Bay where this sponge occurs. The characterization of these novel planctomycetes revealed that cells of one unique strain do not possess condensed nucleoids, a phenotype distinct from other planctomycetes. In addition, a culture-independent clone library approach identified unique planctomycete 16S rRNA gene sequences closely related to other sponge-derived sequences. The analysis of tissue of the sponge Niphates sp. showed that the mesohyl of the sponge is almost devoid of microbial cells, indicating this species is in the group of ‘low microbial abundant’ (LMA) sponges. The unique planctomycete 16S rRNA gene sequences identified in this study were phylogenetically closely related to sequences from LMA sponges in other published studies. This study has revealed new insights into the diversity of planctomycetes in the marine environment and the association of planctomycetes with marine sponges.

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

Similar content being viewed by others

References

  • Bengtsson MM, Øvreås L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261

    Article  PubMed  Google Scholar 

  • Chouari R, Le Paslier D, Daegelen P, Ginestet P, Weissenbach J, Sghir A (2003) Molecular evidence for novel planctomycete diversity in a municipal wastewater treatment plant. Appl Environ Microbiol 69:7354–7363

    Article  PubMed  CAS  Google Scholar 

  • Delong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934

    Article  Google Scholar 

  • Derakshani M, Lukow T, Liesack W (2001) Novel bacterial lineages at the (sub)division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms. Appl Environ Microbiol 67:623–631

    Article  PubMed  CAS  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Keller K et al (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W394–W399

    Article  PubMed  CAS  Google Scholar 

  • Egert M, Wagner B, Lemke T, Brune A, Friedrich MW (2003) Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl Environ Microbiol 69:6659–6668

    Article  PubMed  CAS  Google Scholar 

  • Enticknap JJ, Kelly M, Peraud O, Hill RT (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72:3724–3732

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Fuchsman CA, Staley JT, Oakley BB, Kirkpatrick JB, Murray JW (2012) Free-living and aggregate-associated Planctomycetes in the Black Sea. FEMS Microbiol Ecol 80:402–416

    Article  PubMed  CAS  Google Scholar 

  • Fuerst JA (2005) Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 59:299–328

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fuerst JA, Gwilliam HG, Lindsay M, Lichanska A, Belcher C, Vickers JE, Hugenholtz P (1997) Isolation and molecular identification of planctomycete bacteria from postlarvae of the giant tiger prawn, Penaeus monodon. Appl Environ Microbiol 63:254–262

    PubMed  CAS  Google Scholar 

  • Gade D, Schlesner H, Glöckner FO, Amann R, Pfeiffer S, Thomm A (2004) Identification of planctomycetes with order-, genus-, and strain-specific 16S rRNA-targeted probes. Microb Ecol 47:243–251

    Article  PubMed  CAS  Google Scholar 

  • Giles EC, 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 83:232–241

    Article  PubMed  CAS  Google Scholar 

  • Glöckner FO, Kube M, Bauer M et al (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298–8303

    Article  PubMed  Google Scholar 

  • Griepenburg U, Ward-Rainey N, Mohamed S et al (1999) Phylogenetic diversity, polyamine pattern and DNA base composition of members of the order Planctomycetales. Int J Syst Bacteriol 49:689–696

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS, Bhandari V, Naushad HS (2012) Molecular signatures for the PVC clade (Planctomycetes, Verrucomicrobia, Chlamydiae, and Lentisphaerae) of bacteria provide insights into evolutionary relationships. Front Microbiol 3:327

    PubMed  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  PubMed  CAS  Google Scholar 

  • Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, Horn M (2003) Microbial diversity of marine sponges. In: Müller WEG (ed) Marine molecular biotechnology. Springer, Berlin, pp 59–88

    Google Scholar 

  • Hobot JA, Villiger W, Escaig J, Maeder M, Ryter A, Kellenberger E (1985) Shape and fine-structure of nucleoids observed on sections of ultrarapidly frozen and cryosubstituted bacteria. J Bacteriol 162:960–971

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Jogler C, Waldmann J, Huang X, Jogler M, Glöckner FO, Mascher T, Kolter R (2012) Identification of proteins likely to be involved in morphogenesis, cell division, and signal transduction in Planctomycetes by comparative genomics. J Bacteriol 194:6419–6430

    Article  PubMed  CAS  Google Scholar 

  • Lage OM, Bondoso J (2011) Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 78:366–375

    Article  PubMed  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Goodfellow M, Stackebrandt E (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Lee KC, Webb RI, Janssen PH, Sangwan P, Romeo T, Staley JT, Fuerst JA (2009a) Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol 9:5

    Article  PubMed  Google Scholar 

  • Lee KC, Webb RI, Fuerst JA (2009b) The cell cycle of the planctomycete Gemmata obscuriglobus with respect to cell compartmentalization. BMC Cell Biol 10:4

    Article  PubMed  Google Scholar 

  • Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175:413–429

    Article  PubMed  CAS  Google Scholar 

  • Lonhienne TGA, Sagulenko E, Webb RI et al (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 107:12883–12888

    Article  PubMed  CAS  Google Scholar 

  • Mohamed NM, Saito K, Tal Y, Hill RT (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4:38–48

    Article  PubMed  CAS  Google Scholar 

  • Morris RM, Longnecker K, Giovannoni SJ (2006) Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ Microbiol 8:1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Neufeld JD, Mohn WW (2006) Assessment of microbial phylogenetic diversity based on environmental nucleic acids. In: Stackebrandt E (ed) Molecular identification, systematics, and population structure of prokaryotes. Springer, Berlin, pp 219–259

    Chapter  Google Scholar 

  • Pimentel-Elardo S, Wehrl M, Friedrich AB, Jensen PR, Hentschel U (2003) Isolation of planctomycetes from Aplysina sponges. Aquat Microb Ecol 33:239–245

    Article  Google Scholar 

  • Pizzetti I, Fuchs BM, Gerdts G, Wichels A, Wiltshire KH, Amann R (2011) Temporal variability of coastal Planctomycetes clades at Kabeltonne station, North Sea. Appl Environ Microbiol 77:5009–5017

    Article  PubMed  CAS  Google Scholar 

  • Reynaud EG, Devos DP (2011) Transitional forms between the three domains of life and evolutionary implications. Proc Biol Sci 278:3321–3328

    Article  PubMed  Google Scholar 

  • Santarella-Mellwig R, Franke J, Jaedicke A et al (2010) The compartmentalized bacteria of the PlanctomycetesVerrucomicrobiaChlamydiae superphylum have membrane coat-like proteins. PLoS Biol 8:e1000281

    Article  PubMed  Google Scholar 

  • Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj IW, Devos DP (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11:e1001565

    Article  PubMed  CAS  Google Scholar 

  • Schattenhofer M, Fuchs BM, Amann R, Zubkov MV, Tarran GA, Pernthaler J (2009) Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ Microbiol 11:2078–2093

    Article  PubMed  CAS  Google Scholar 

  • Schlesner H (1994) The development of media suitable for the microorganisms morphologically resembling Planctomyces spp, Pirellula spp, and other Planctomycetales from various aquatic habitats using dilute media. Syst Appl Microbiol 17:135–145

    Article  Google Scholar 

  • Schlesner H, Rensmann C, Tindall BJ, Gade D, Rabus R, Pfeiffer S, Hirsch P (2004) Taxonomic heterogeneity within the Planctomycetales as derived by DNA–DNA hybridization, description of Rhodopirellula baltica gen. nov., sp nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov as Blastopirellula marina comb. nov and emended description of the genus Pirellula. Int J Syst Evol Microbiol 54:1567–1580

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Schmitt S, Tsai P, Bell J et al (2011) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576

    Article  PubMed  Google Scholar 

  • Simister RL, Deines P, Botte ES, Webster NS, Taylor MW (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14:517–524

    Article  PubMed  CAS  Google Scholar 

  • Sipkema D, Holmes B, Nichols SA, Blanch HW (2009) Biological characterisation of Haliclona (?gellius) sp.: sponge and associated microorganisms. Microb Ecol 58:903–920

    Article  PubMed  CAS  Google Scholar 

  • Sipkema D, Schippers K, Maalcke WJ, Yang Y, Salim S, Blanch HW (2011) Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (gellius) sp. Appl Environ Microbiol 77:2130–2140

    Article  PubMed  CAS  Google Scholar 

  • Speth DR, van Teeseling MCF, Jetten MSM (2012) Genomic analysis indicates the presence of an asymmetric bilayer outer membrane in Planctomycetes and Verrucomicrobia. Front Microbiol 3:304

    PubMed  Google Scholar 

  • Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16s rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  • Staley JT, Marshall KC, Skerman VBD (1980) Budding and prosthecate bacteria from fresh-water habitats of various trophic states. Microb Ecol 5:245–251

    Article  Google Scholar 

  • Sunagawa S, Woodley CM, Medina M (2010) Threatened corals provide underexplored microbial habitats. PLoS One 5:e9554

    Article  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  PubMed  CAS  Google Scholar 

  • Taylor MW, Tsai P, Simister RL et al (2012) ‘Sponge-specific’ bacteria are widespread (but rare) in diverse marine environments. ISME J. doi:10.1038/ismej.2012.111

    Google Scholar 

  • Thiel V, Neulinger SC, Staufenberger T, Schmaljohann R, Imhoff JF (2007) Spatial distribution of sponge-associated bacteria in the Mediterranean sponge Tethya aurantium. FEMS Microbiol Ecol 59:47–63

    Article  PubMed  CAS  Google Scholar 

  • Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence based PCR (rep-PCR). Methods Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  • Vidgen ME, Hooper JNA, Fuerst JA (2012) Diversity and distribution of the bioactive actinobacterial genus Salinispora from sponges along the Great Barrier Reef. Antonie Van Leeuwenhoek 101:603–618

    Article  PubMed  CAS  Google Scholar 

  • Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17:241–249

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Jenkins C, Webb RI, Fuerst JA (2002) Isolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater. Appl Environ Microbiol 68:417–422

    Article  PubMed  CAS  Google Scholar 

  • Ward N, Staley JT, Fuerst JA, Giovannoni S, Schlesner H, Stackebrandt E (2006) The order Planctomycetales, including the genera Planctomyces, Pirellula, Gemmata and Isosphaera and the Candidatus genera Brocadia, Kuenenia and Scalindua. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Proteobacteria: delta, Epsilon subclass, vol 7. Springer, New York, pp 757–793

    Chapter  Google Scholar 

  • Webster NS, Bourne D (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiol Ecol 59:81–94

    Article  PubMed  CAS  Google Scholar 

  • Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444

    Article  PubMed  CAS  Google Scholar 

  • Winkelmann N, Harder J (2009) An improved isolation method for attached-living Planctomycetes of the genus Rhodopirellula. J Microbiol Methods 77:276–284

    Article  PubMed  CAS  Google Scholar 

  • Woebken D, Teeling H, Wecker P et al (2007) Fosmids of novel marine Planctomycetes from the Namibian and Oregon coast upwelling systems and their cross-comparison with planctomycete genomes. ISME J 1:419–435

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Li Z (2012) Spatial distribution of prokaryotic symbionts and ammoxidation, denitrifier bacteria in marine sponge Astrosclera willeyana. Sci Rep 2:528

    PubMed  Google Scholar 

  • Yee B, Sagulenko E, Fuerst JA (2011) Making heads or tails of the HU proteins in the planctomycete Gemmata obscuriglobus. Microbiology 157:2012–2021

    Article  PubMed  CAS  Google Scholar 

  • Yee B, Sagulenko E, Morgan GP, Webb RI, Fuerst JA (2012) Electron tomography of the nucleoid of Gemmata obscuriglobus reveals complex liquid crystalline cholesteric structure. Front Microbiol 3:326

    Article  PubMed  Google Scholar 

  • Zhu P, Li QZ, Wang GY (2008) Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. Microb Ecol 55:406–414

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Research on planctomycetes in the laboratory of J.A.F. was funded by an Australian Research Council Discovery Project. We thank Dr Merrick Ekins, Dr Patricia Sutcliffe, and Dr John Hooper at Queensland Museum for the identification of the sponge Niphates sp.; Dr Kathy Townsend at Moreton Bay Research Station for her assistance in the collection of the sponge specimens; and Marinova Pty Ltd (Tasmania, Australia) for donation of a fucoidan sample. H.I was supported by the University of Queensland Research Scholarship (UQRS) and University of Queensland International Research Tuition Award (UQIRTA).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroshi Izumi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Izumi, H., Sagulenko, E., Webb, R.I. et al. Isolation and diversity of planctomycetes from the sponge Niphates sp., seawater, and sediment of Moreton Bay, Australia. Antonie van Leeuwenhoek 104, 533–546 (2013). https://doi.org/10.1007/s10482-013-0003-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-013-0003-5

Keywords

Navigation