Skip to main content

Advertisement

Springer Nature Link
Log in

Genetic and phenotypic evidence for Streptomyces griseus ecovars isolated from a beach and dune sand system

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

Abstract

This study was designed to determine the biogeography of six alkaliphilic Streptomyces strains which had been isolated from four locations within a 60 m transect across a beach and dune sand system. The six strains shared >99% 16S rRNA gene similarities with one another and with representative strains of Streptomyces griseus. Infraspecific diversity amongst the strains was investigated by multilocus sequence typing (MLST) in combination with carbon utilisation phenotypic testing. The results show that each of the strains is genotypically and phenotypically distinct. Furthermore, the MLST and carbon utilisation profiles were congruent thereby providing preliminary evidence which suggests that the observed infraspecific diversity is consistent with ecological selection. The results also demonstrate that infraspecific diversity can be observed over small spatial scales. These findings support the hypothesis that the six isolates are ecovars of Streptomyces griseus. The implications of these findings for prokaryotic biogeography and bioprospecting are discussed.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Antony-Babu S, Goodfellow M (2008) Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune sand system. Antonie Van Leeuwenhoek (submitted)

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D and 33 other authors (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

  • Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26

    PubMed  Google Scholar 

  • Breslauer KJ, Frank R, Blöcher H, Marky LA (1986) Predicting DNA duplex stability from the base sequence. Proc Natl Acad Sci 83:3746–3750

    Article  PubMed  CAS  Google Scholar 

  • Bruntner C, Binder T, Pathom-aree W, Goodfellow M, Bull AT, Potterat O, Puder C, Schmid A, Bolek W (2005) Frigocyclonine, a novel angucyclinone antibiotic produced by a Streptomyces griseus strain from Antarctica. J Antibiot 58:346–349

    PubMed  CAS  Google Scholar 

  • Bull AT, Ward AC, Goodfellow M (2000) Search and discovery strategies for biotechnology: the paradigm shift. Microbiol Mol Rev 64:573–606

    Article  CAS  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the CLUSTAL series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed  CAS  Google Scholar 

  • Cho JC, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66:5448–5456

    Article  PubMed  CAS  Google Scholar 

  • Chun J (1995) Computer-assisted classification and identification of actinomycetes. Department of Agriculture and Environmental Sciences, University of Newcastle, Newcastle-upon-Tyne

    Google Scholar 

  • Coenye T, Gevers D, Van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29:147–167

    Article  PubMed  CAS  Google Scholar 

  • Cohan FM (2002) What are bacterial species? Annu Rev Microbiol 56:457–487

    Article  PubMed  CAS  Google Scholar 

  • Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Springs

    Google Scholar 

  • Fenchel T (2003) Biogeography for bacteria. Science 301:925–926

    Article  PubMed  CAS  Google Scholar 

  • Fenchel T, Esteban GF, Finlay BJ (1997) Local versus global diversity of microorganisms: cryptic diversity of ciliated protozoa. Oikos 80:220–225

    Article  Google Scholar 

  • Fiedler HP, Bruntner C, Bull AT, Ward AC, Goodfellow M, Potterat O, Puder C, Mihm G (2005) Marine actinomycetes as a source of novel secondary metabolites. Antonie Van Leeuwenhoek 87:37–42

    Article  PubMed  CAS  Google Scholar 

  • Findlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063

    Article  Google Scholar 

  • Fox GE, Wisotzkey JD, Jurtshuk P Jr (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Evol Microbiol 42:166–170

    CAS  Google Scholar 

  • Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Fell EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739

    Article  PubMed  CAS  Google Scholar 

  • Goodfellow M, Manfio GP, Chun J (1997) Towards a practical species concept for cultivable bacteria. In: Claridge MF, Dawah HA, Wilson MR (eds) Species: the units of biodiversity. Chapman & Hall, London, pp 25–59

    Google Scholar 

  • Goodfellow M, Kumar Y, Labeda DP, Sembiring L (2007) The Streptomyces violaceusniger clade: a home for streptomycetes with rugose ornamented spores. Antonie Van Leeuwenhoek 92:173–199

    Article  PubMed  Google Scholar 

  • Graf E, Schneider K, Nicholson G, Ströbele M, Jones AL, Goodfellow M, Beil W, Süssmuth D, Fiedler H-P (2007) Elloxazinones A and B, new aminophenoxazinones from Streptomyces griseus ACTA 2871. J Antibiot 60:277–284

    PubMed  CAS  Google Scholar 

  • Guo Y, Zheng W, Rong X, Huang Y (2008) A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149–159

    Article  PubMed  CAS  Google Scholar 

  • Hedlund BP, Staley JT (2004) Microbial endemism and biogeography. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, pp 225–231

    Google Scholar 

  • Höltzel A, Dieter A, Schmid DG, Brown R, Goodfellow M, Beil W, Jung G, Fiedler HP (2003) Lactonamycin Z, an antibiotic and antitumor compound provided by Streptomyces sanglieri strain AK 623. J Antibiot 56:1058–1061

    PubMed  Google Scholar 

  • Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Ōmura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531

    Article  PubMed  Google Scholar 

  • Jaccard P (1908) Adaptative hierarchical clustering schemes. Syst Zool 19:58–82

    Google Scholar 

  • Jaspers E, Overmann J (2004) Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70:4831–4839

    Article  PubMed  CAS  Google Scholar 

  • Jensen PR, Mafnas C (2006) Biogeography of the marine actinomycete Salinispora. Environ Microbiol 8:1881–1888

    Article  PubMed  CAS  Google Scholar 

  • Jensen PR, Mincer TJ, Williams PG, Fenical W (2005) Marine actinomycete diversity and natural product discovery. Antonie Van Leeuwenhoek 87:43–48

    Article  PubMed  CAS  Google Scholar 

  • Jensen PR, Williams PG, Oh CD, Zeigler L, Fenical W (2007) Species specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl Environ Microbiol 73:1146–1152

    Article  PubMed  CAS  Google Scholar 

  • Kieser T, Bibb MJ, Buttner M, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation Norwich, UK

    Google Scholar 

  • Kim WY (2004) The Streptomyces violaceoruber clade: a model system for defining a post-genomic species concept for streptomycetes. School of Biology, University of Newcastle, Newcastle-upon-Tyne, UK

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, Ward DM, Rooney AP, Brambilla E, Connor N, Ratcliff RM, Nevo E, Cohan FM (2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci USA 105:2504–2509

    Article  PubMed  CAS  Google Scholar 

  • Korber B (2000) HIV signature and sequence variation analysis. Computational analysis of HIV molecular sequences. In: Rodrigo AG, Learn GH (eds) Computational and evolutionary analysis of HIV molecular sequences. Kluwer Academic Publishers, Boston, pp 55–72

    Google Scholar 

  • Korn F, Weingärtner B, Kutzner HJ (1978) A study of actinophages: morphology, serological relationship and host range. In: Freerksen I, Tárnok I, Thumim JH (eds) Genetics of the Actinomycetales. Gustav Fischer Verlag, Stuttgart, pp 251–270

    Google Scholar 

  • Kumar Y, Aiemsum-ang P, Ward AC, Goodfellow M (2007) Diversity and geographical distribution of members of the Streptomyces violaceusniger 16S rRNA gene clade detected by clade-specific PCR primers. FEMS Microbiol Ecol 62:54–63

    Article  PubMed  CAS  Google Scholar 

  • Larsen TO, Smedsgaard KF, Nielsen KF, Hansen ME, Frisvad JC (2005) Phenotypic taxonomy and metabolite profiling in microbial drug discovery. Nat Prod Rep 22:672–675

    Article  PubMed  CAS  Google Scholar 

  • Majewski J, Cohan FM (1999) Adapt globally, act locally: the effect of selective sweeps on bacterial sequence diversity. Genetics 152:1459–1474

    PubMed  CAS  Google Scholar 

  • Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A (2008) Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214

    Article  PubMed  CAS  Google Scholar 

  • Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Øvreås L, Reysenbach AL, Smith VH (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  PubMed  CAS  Google Scholar 

  • Palys T, Nakamura LK, Cohan FM (1997) Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int J Syst Evol Microbiol 47:1145–1156

    Article  CAS  Google Scholar 

  • Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5:650–659

    Article  PubMed  CAS  Google Scholar 

  • Pathom-aree W, Stach JEM, Ward AC, Horikoshi K, Bull AT, Goodfellow M (2006) Diversity of actinomycetes isolated from Challenger Deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10:181–189

    Article  PubMed  CAS  Google Scholar 

  • Piel J (2004) Metabolites from symbiotic bacteria. Nat Prod Rep 21:519–538

    Article  PubMed  CAS  Google Scholar 

  • Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72

    Article  PubMed  CAS  Google Scholar 

  • Ramette A, Tiedje JM (2007) Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. Microbiol Ecol 5:197–207

    Article  Google Scholar 

  • Rohlf FJ (1988) NTSYS-pc: numerical taxonomy and multivariate analysis system, version 2.0, user guide. Exeter Software, New York

    Google Scholar 

  • Rossellö-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  PubMed  Google Scholar 

  • Saitou N, Imanashi T (1989) Relative efficiencies of the Fitch-Margoliash, maximum-parsimony, maximum-likehood, minimum-evolution, and neighbor-joining methods of phylogenetic tree construction in obtaining the correct tree. Mol Biol Evol 6:514–525

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sembiring L, Ward AC, Goodfellow M (2000) Selective isolation and characterisation of members of the Streptomyces violaceusniger clade associated with the roots of Paraserianthes falcataria. Antonie Van Leeuwenhoek 78:353–366

    Article  PubMed  CAS  Google Scholar 

  • Sneath PHA, Sokal RR (eds) (1973) Numerical taxonomy: the principles and practice of numerical classification. W.H. Freeman and Co., San Francisco

    Google Scholar 

  • Sokal RR, Michener CD (1958) A statistical method for evaluating systematic relationships. Kansas Univ Sci Bull 38:1409–1438

    Google Scholar 

  • Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MCJ, Nesme X, Rosselló-Mora R, Swings J, Trüper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047

    Article  PubMed  CAS  Google Scholar 

  • Staley JT, Gosink JJ (1999) Poles apart: biodiversity and biogeography of sea ice bacteria. Annu Rev Microbiol 53:189–215

    Article  PubMed  CAS  Google Scholar 

  • Strohl W (2004) Antimicrobials. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, pp 288–313

    Google Scholar 

  • Thompson FL, Gevers D, Thompson CC, Davyndt P, Naser S, Hoste B, Munn CB, Swings F (2005) Phylogeny and molecular identification on the basis of multilocus sequence analysis. Appl Environ Microbiol 71:5107–5115

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  PubMed  CAS  Google Scholar 

  • Ward AC, Goodfellow M (2004) Phylogeny and functionality: taxonomy as a roadmap to genes. In: Bull AT (ed) Microbial diversity and bioprospecting. ASP Press, Washington, pp 288–313

    Google Scholar 

  • Watve MG, Tickoo R, Jog MM, Bhole BD (2001) How many antibiotics are produced by the genus Streptomyces? Arch Microbiol 176:386–390

    Article  PubMed  CAS  Google Scholar 

  • Whitaker RJ (2006) Allopatric origins of microbial species. Philos Trans Roy Soc B 361:1975–1984

    Article  Google Scholar 

  • Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978

    Article  PubMed  CAS  Google Scholar 

  • Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Sanjay Antony-Babu is grateful to the University of Newcastle for the award of an International Research Scholarship and to the School of Biology for a Research Studentship.

Author information

Authors and Affiliations

  1. School of Biology, Newcastle University, Newcastle-upon-Tyne, NE1 7RU, UK

    Sanjay Antony-Babu, James E. M. Stach & Michael Goodfellow

Authors
  1. Sanjay Antony-Babu
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. James E. M. Stach
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Michael Goodfellow
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Sanjay Antony-Babu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Antony-Babu, S., Stach, J.E.M. & Goodfellow, M. Genetic and phenotypic evidence for Streptomyces griseus ecovars isolated from a beach and dune sand system. Antonie van Leeuwenhoek 94, 63–74 (2008). https://doi.org/10.1007/s10482-008-9246-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-008-9246-y

Keywords