Skip to main content
SpringerLink
Log in

Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune sand system

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

Abstract

Alkaliphilic streptomycetes were isolated from composite sand samples collected from six out of seven locations across a beach and dune sand system using starch-casein-nitrate agar supplemented with cycloheximide and buffered to pH 10.5. The isolates had colonial and chemotaxonomic properties consistent with their classification in the genus Streptomyces. They were assigned to 49 multimembered and 114 single-membered colour-groups given their ability to produce pigments on oatmeal and peptone-yeast-extract-iron agars and to corresponding taxa based on whole-genome rep-PCR banding patterns. Twenty-four isolates representing the colour and rep-PCR groups grew well from pH 5 to 11, and optimally at pH 9, as did phylogenetically close members of the Streptomyces griseus 16S rRNA gene clade. One hundred and twelve representative alkaliphilic streptomycetes formed a heterogeneous but distinct clade in the Streptomyces 16S rRNA gene tree. A 3-dimensional representation of 16S rRNA sequence data showed that the alkaliphilic streptomycetes formed a distinct group in multidimensional taxospace. It is evident that alkaliphilic streptomycetes are common in the beach and dune sand system and that representatives of this community form new centers of taxonomic variation within the genus Streptomyces that can be equated with species.

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

Similar content being viewed by others

References

  • Anderson AS, Wellington EMH (2001) The taxonomy of Streptomyces and related genera. Int J Syst Evol Microbiol 51:797–814

    PubMed  CAS  Google Scholar 

  • Antony-Babu S, Okorafor LA, Stach JEM, Goodfellow M (2007) Alkaliphilic streptomycetes: prospective new candidates for bioprospecting. In: Proceedings of the 14th international symposium on the biology of actinomycetes, University of Newcastle, UK, p 110

  • Atalan E, Manfio GP, Ward AC, Kroppenstedt RM, Goodfellow M (2000) Biosystematic studies on novel streptomycetes from soil. Antonie Van Leeuwenhoek 77:337–353. doi:10.1023/A:1002682728517

    Article  PubMed  CAS  Google Scholar 

  • Basilio A, Gonzalez I, Vicente MF, Gorrochategui J, Cabello A, Gonzalez A et al (2003) Patterns of antimicrobial activities from soil actinomycetes isolated under different conditions of pH and salinity. J Appl Microbiol 95:814–823. doi:10.1046/j.1365-2672.2003.02049.x

    Article  PubMed  CAS  Google Scholar 

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM et al (2002) Complete genome sequence of the model actinomycete “Streptomyces coelicolor A3(2)”. Nature 417:141–147. doi:10.1038/417141a

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • British Standards Institution (1995) Soil quality. Chemical methods. Determination of organic and total carbon after dry combustion (elementary analysis). British Standard 7755-3.8. British Standards Institution, London

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

    CAS  Google Scholar 

  • Bull AT, Stach JEM, Ward AC, Goodfellow M (2005) Marine actinobacteria: perspectives, challenges, future directions. Antonie Van Leeuwenhoek 87:65–79. doi:10.1007/s10482-004-6562-8

    Article  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 

  • Dieter A, Hamm A, Fiedler HP, Goodfellow M, Műller WEG, Brun R et al (2003) Pyrocoll, an antibiotic, antiparasitic and antitumor compound produced by a novel alkaliphilic Streptomyces strain. J Antibiot 56:639–646

    CAS  Google Scholar 

  • Duangmal K, Ward AC, Goodfellow M (2005) Selective isolation of members of the Streptomyces violaceoruber clade from soil. FEMS Microbiol Lett 245:321–327. doi:10.1016/j.femsle.2005.03.028

    Article  PubMed  CAS  Google Scholar 

  • Fahmy T, Aubry P (2003) XLSTAT-pro, version 7.0, Paris

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol Int J Org Evol 39:783–791. doi:10.2307/2408678

    Google Scholar 

  • Fiedler HP, Bruntner C, Bull AT, Ward AC, Goodfellow M, Potterat O et al (2005) Marine actinomycetes as a source of novel secondary metabolites. Antonie Van Leeuwenhoek 87:37–42. doi:10.1007/s10482-004-6538-8

    Article  PubMed  CAS  Google Scholar 

  • Goodfellow M, Dawson D (1978) Qualitative and quantitative studies of bacteria colonizing Picea sitchensis litter. Soil Biol Biochem 10:303–307. doi:10.1016/0038-0717(78)90027-5

    Article  Google Scholar 

  • Goodfellow M, Haynes JA (1984) Actinomycetes in marine sediments. In: Ortiz-Ortiz L, Bojalil LF, Yakoleff V (eds) Biological and biomedical aspects of actinomycetes. Academic Press, New York, pp 452–472

    Google Scholar 

  • Goodfellow M, Ferguson EV, Sanglier JJ (1992) Numerical classification and identification of Streptomyces species—a review. Gene 115:225–233. doi:10.1016/0378-1119(92)90563-5

    Article  PubMed  CAS  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. doi:10.1007/s10482-007-9146-6

    Article  PubMed  Google Scholar 

  • Graf E, Schneider K, Nicholson G, Ströbele M, Jones AL, Goodfellow M et al (2007) Elloxazinones A and B, new aminophenoxazinones from Streptomyces griseus Acta 2871. J Antibiot 60:277–284

    PubMed  CAS  Google Scholar 

  • Häne BG, Jäger K, Drexler H (1993) The Pearson product-moment correlation coefficient is better suited for identification of DNA fingerprint profiles than band matching algorithms. Electrophoresis 14:967–972. doi:10.1002/elps.11501401154

    Article  PubMed  Google Scholar 

  • He L, Li W, Huang Y, Wang L, Liu Z, Lanoot B et al (2005) Streptomyces jietaisiensis sp. nov., isolated from soil in northern China. Int J Syst Bacteriol 55:1939–1944

    CAS  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

  • Hozzein WN, Ali MIA, Hammouda O, Mousa AS, Li W-J, Xu L-H et al (2008) Streptomyces sannurensis sp. nov., a novel alkaliphilic streptomycete isolated from Wadi Sannur in Egypt. Antonie Van Leeuwenhoek (in press)

  • Huang Y, Li W, Wang L, Lanoot B, Vancanneyt M, Rodriguez C et al (2004) Streptomyces glauciniger sp. nov., a novel mesophilic streptomycete isolated from soil in south China. Int J Syst Evol Microbiol 54:2085–2089. doi:10.1099/ijs.0.63158-0

    Article  PubMed  CAS  Google Scholar 

  • Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T et al (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531. doi:10.1038/nbt820

    Article  PubMed  Google Scholar 

  • Jones KL (1949) Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141–145

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–123

    Google Scholar 

  • Kelly KL (1964) Inter-Society Color Council–National Bureau of Standards Color-Name Charts Illustrated with Centroid Colors. US Government Printing Office, Washington, DC

  • Kieser T, Bibb MJ, Buttner M, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich, pp 162–170

    Google Scholar 

  • Kim B, Sahin N, Minnikin DE, Zakrzewska-Czerwinska J, Mordarski M, Goodfellow M (1999) Classification of thermophilic streptomycetes, including the description of Streptomyces thermoalcalitolerans sp. nov. Int J Syst Evol Microbiol 49:7–17

    Article  Google Scholar 

  • Kim SB, Seong CN, Jeon SJ, Bae KS, Goodfellow M (2004) Taxonomic study of neutrotolerant acidophilic actinomycetes isolated from soil and description of Streptomyces yeochonensis sp. nov. Int J Syst Evol Microbiol 54:211–214. doi:10.1099/ijs.0.02519-0

    Article  PubMed  CAS  Google Scholar 

  • Kumar Y, Goodfellow M (2008) Five new species of the Streptomyces violaceusniger 16S rRNA gene clade: Streptomyces castelarensis comb. nov., Streptomyces himastatinicus sp. nov., Streptomyces mordarskii sp. nov., Streptomyces rapamycinicus sp. nov. and Streptomyces ruanii sp. nov. Int J Syst Evol Microbiol (in press)

  • Kűster E, Williams ST (1964) Selection of media for isolation of streptomycetes. Nature 202:928–929. doi:10.1038/202928a0

    Article  Google Scholar 

  • Lanoot B, Vancanneyt M, Hoste B, Vandemeulebroecke K, Cnockaert MC, Dawyndt P et al (2005) Grouping of streptomycetes using 16S-ITS RFLP fingerprinting. Res Microbiol 156:755–762. doi:10.1016/j.resmic.2005.01.017

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Shi Y, Zhang Y, Zhou Z, Lu Z, Li W et al (2005) Classification of Streptomyces griseus (Krainsky 1914) Waksman and Henrici 1948 and related species and the transfer of ‘Microstreptospora cinerea’ to the genus Streptomyces as Streptomyces yanii sp. nov. Int J Syst Evol Microbiol 55:1605–1610. doi:10.1099/ijs.0.63654-0

    Article  PubMed  CAS  Google Scholar 

  • Manfio GP, Zakrzewska-Czerwinska J, Atalan E, Goodfellow M (1995) Towards minimal standards for description of Streptomyces species. Biotechnologia 7:242–283

    Google Scholar 

  • Manfio GP, Atalan E, Zakrzewska-Czerwinska J, Mordarski M, Rodriguez C, Collins MD et al (2003) Classification of novel soil streptomycetes as Streptomyces aureus sp. nov., Streptomyces laceyi sp. nov. and Streptomyces sanglieri sp. nov. Antonie Van Leeuwenhoek 83:245–255. doi:10.1023/A:1023332427794

    Article  PubMed  CAS  Google Scholar 

  • Mao J, Tang Q, Zhang Z, Wang W, Wei D, Huang Y et al (2007) Streptomyces radiopugnans sp. nov., a radiation-resistant actinomycete isolated from radiation-polluted soil in China. Int J Syst Evol Microbiol 57:2578–2582. doi:10.1099/ijs.0.65027-0

    Article  PubMed  CAS  Google Scholar 

  • Mehta VJ, Thumar JT, Singh SP (2006) Production of alkaline protease from an alkaliphilic actinomycete. Bioresour Technol 97:1650–1654. doi:10.1016/j.biortech.2005.07.023

    Article  PubMed  CAS  Google Scholar 

  • Mikami Y, Miyashita K, Arai T (1982) Diaminopimelic acid profiles of alkalophilic and alkaline-resistant strains of actinomycetes. J Gen Microbiol 128:1709–1712

    PubMed  CAS  Google Scholar 

  • Ōmura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M et al (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci USA 98:22215–12220

    Google Scholar 

  • Pridham TG, Tresner HD (1974) Genus I. Streptomyces Waksman and Henrici 1943, 339. In: Buchanan RE, Gibbons NE (eds) Bergey’s manual of determinative bacteriology. The Williams and Wilkins Co., Baltimore, pp 748–829

    Google Scholar 

  • Reed JF, Cummings RW (1945) Soil reaction-glass electrodes and colorimetric methods for determining pH values in soil. Soil Sci 59:97–104. doi:10.1097/00010694-194501000-00015

    Article  CAS  Google Scholar 

  • Rohlf FJ (1988) NTSYS-pc: numerical taxonomy and multivariate analysis system. Applied Biostatistics Inc., Setauket

    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. doi:10.1023/A:1010226515202

    Article  PubMed  CAS  Google Scholar 

  • Seong CN, Goodfellow M, Ward AC, Hah YC (1993) Numerical classification of acidophilic actinomycetes isolated from acid soil in Korea. Korean J Microbiol 31:355–363

    CAS  Google Scholar 

  • Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313

    Google Scholar 

  • Solingen P, Meijer D, Kleij WA, Barnett C, Bolle R, Power SD et al (2001) Cloning and expression of an endocellulase gene from a novel streptomycete isolated from an East African soda lake. Extremophiles 5:333–341. doi:10.1007/s007920100198

    Article  PubMed  Google Scholar 

  • Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Environ Microbiol 28:226–231

    CAS  Google Scholar 

  • Strohl WR (2004) Antimicrobials. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, DC, pp 336–355

    Google Scholar 

  • Taber WA (1960) Evidence for the existence of acid-sensitive actinomycetes in soil. Can J Microbiol 6:503–514

    Article  Google Scholar 

  • Van de Peer Y, De Wachter R (1994) Treecon for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    PubMed  Google Scholar 

  • Vasavada SH, Thumar JT, Singh SP (2006) Secretion of a potent antibiotic by salt-tolerant and alkaliphilic actinomycete Streptomyces sannanensis strain RJT-1. Curr Sci 91:1393–1397

    CAS  Google Scholar 

  • Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831. doi:10.1093/nar/19.24.6823

    Article  PubMed  CAS  Google Scholar 

  • Vickers JC, Williams ST, Ross GW (1984) A taxonomic approach to selective isolation of streptomycetes from soil. In: Ortiz-Ortiz L, Bojalil LF, Yakoleff V (eds) Biological biochemical and biomedical aspects of actinomycetes. Academic Press, London, pp 553–561

    Google Scholar 

  • Watson ET, Williams ST (1974) Studies on ecology of actinomycetes in soil. VII. Actinomycetes in a coastal sand belt. Soil Biol Biochem 6:43–52. doi:10.1016/0038-0717(74)90010-8

    Article  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. doi:10.1007/s002030100345

    Article  PubMed  CAS  Google Scholar 

  • Williams ST, Vickers JC (1988) Detection of actinomycetes in the natural environment: problems and perspectives. In: Okami Y, Beppu T, Ogawara K (eds) Biology of actinomycetes. Japan Scientific Societies Press, Tokyo, pp 265–270

    Google Scholar 

  • Williams ST, Davies FL, Mayfield CI, Khan MR (1971) Studies on the ecology of actinomycetes in soil. II. The pH requirements of streptomycetes from two acid soils. Soil Biol Biochem 3:187–195. doi:10.1016/0038-0717(71)90014-9

    Article  CAS  Google Scholar 

  • Williams ST, Lanning S, Wellington EMH (1984) Ecology of actinomycetes. In: Goodfellow M, Mordarski M, Williams ST (eds) The biology of the actinomycetes. Academic Press, Inc., London, pp 481–528

    Google Scholar 

  • Xu C, Wang L, Cui Q, Huang Y, Liu Z, Zhang G et al (2006) Novel neutrotolerant acidophilic Streptomyces species isolated from acidic soils in China: Streptomyces guandensis sp. nov., Streptomyces paucisporeus sp. nov., Streptomyces rubidus sp. nov. and Streptomyces yanglinensis sp. nov. Int J Syst Evol Bacteriol 56:1109–1115

    CAS  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

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

    Sanjay Antony-Babu & Michael Goodfellow

Authors
  1. Sanjay Antony-Babu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Goodfellow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sanjay Antony-Babu.

Additional information

GenBank accession numbers for the 16S rRNA gene sequences for the strains of the alkaliphilic streptomycetes Bd 095, Bd 064, Bd 077, Bd 013, Bd 108, Bd 088, Bd 012, Bd 187, Bd 128, Bd 174, Bd 167, Lt 005, Lt 006, Fd 015, Bd 099, Bd 059, Bd 159, Ht 015, Md 005, Ht 020, Bd 205, Md 063, Fd 004, Md 039 and Bd 092 are EU477215, EU477216, EU477217, EU477218, EU477219, EU477220, EU477221, EU477222, EU477223, EU477224, EU477225, EU477226, EU477227, EU477228, EU477229, EU477230, EU477231, EU477232, EU477233, EU477234, EU477235, EU477236, EU477237, EU477238 and EU477257, respectively.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Antony-Babu, S., Goodfellow, M. Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune sand system. Antonie van Leeuwenhoek 94, 581–591 (2008). https://doi.org/10.1007/s10482-008-9277-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-008-9277-4

Keywords

Search

Navigation