Skip to main content
Log in

Phylogenetic study of the species within the family Streptomycetaceae

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

Abstract

Species of the genus Streptomyces, which constitute the vast majority of taxa within the family Streptomycetaceae, are a predominant component of the microbial population in soils throughout the world and have been the subject of extensive isolation and screening efforts over the years because they are a major source of commercially and medically important secondary metabolites. Taxonomic characterization of Streptomyces strains has been a challenge due to the large number of described species, greater than any other microbial genus, resulting from academic and industrial activities. The methods used for characterization have evolved through several phases over the years from those based largely on morphological observations, to subsequent classifications based on numerical taxonomic analyses of standardized sets of phenotypic characters and, most recently, to the use of molecular phylogenetic analyses of gene sequences. The present phylogenetic study examines almost all described species (615 taxa) within the family Streptomycetaceae based on 16S rRNA gene sequences and illustrates the species diversity within this family, which is observed to contain 130 statistically supported clades, as well as many unsupported and single member clusters. Many of the observed clades are consistent with earlier morphological and numerical taxonomic studies, but it is apparent that insufficient variation is present in the 16S rRNA gene sequence within the species of this family to permit bootstrap-supported resolution of relationships between many of the individual clusters.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • A co-operative study, Gottlieb D (1961) An evaluation of criteria and procedures used in the description and characterization of the streptomycetes. Appl Microbiol 9:55–65

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bouchek-Mechiche K, Gardan L, Andrivon D, Normand P (2006) Streptomyces turgidiscabies and Streptomyces reticuliscabiei: one genomic species, two pathogenic groups. Int J Syst Evol Microbiol 56:2771–2776

    Article  PubMed  CAS  Google Scholar 

  • Chun J, Goodfellow M (1995) A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Bacteriol 45:240–245

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Felsenstein J (1993) Phylogeny inference package (PHYLIP) version 3.5. University of Washington, Seattle

    Google Scholar 

  • Ferguson EV, Ward AC, Sanglier J-J, Goodfellow M (1997) Evaluation of Streptomyces species-groups by pyrolysis mass spectrometry. Zbl Bakt 285:169–181

    CAS  Google Scholar 

  • Goodfellow M, Williams ST, Alderson G (1986a) Transfer of Elytrosporangium brasiliense Falcão de Morais et al., Elytrosporangium spirale Falcão de Morais et al., Microellobosporia flava Cross et al., Microellobosporia grisea (Konev et al.) Pridham and Microellobosporia violacea (Tsyganov et al.) Pridham to the genus Streptomyces, with emended descriptions of the species. Syst Appl Microbiol 8:48–54

    Article  Google Scholar 

  • Goodfellow M, Williams ST, Alderson G (1986b) Transfer of Chainia species to the genus Streptomyces with emended description of species. Syst Appl Microbiol 8:55–60

    Article  Google Scholar 

  • Goodfellow M, Williams ST, Alderson G (1986c) Transfer of Actinosporangium violaceum Krasil’nikov and Yuan, Actinosporangium vitaminophilum Shomura et al. and Actinopycridium caeruleum Krasil’nikov to the genus Streptomyces, with emended descriptions of the species. Syst Appl Microbiol 8:61–64

    Article  Google Scholar 

  • Goodfellow M, Williams ST, Alderson G (1986d) Transfer of Kitasatoa purpurea Matsumae and Hata to the genus Streptomyces as Streptomyces purpureus comb. nov. Syst Appl Microbiol 8:65–66

    Article  Google Scholar 

  • Goodfellow M, Ferguson EV, Sanglier J-J (1992) Numerical classification and identification of Streptomyces species—a review. Gene 115:225–233

    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 92:173–197

    Article  PubMed  Google Scholar 

  • Gottlieb D (1963) Recommendations for description of some Actinomycetales appearing in patent applications. Int Bull Bacteriol Nomencl Taxon 13:159–160

    Article  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 

  • Hall TA (1999) BioEdit, a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Kämpfer P (2011) Genus Streptomyces Waksman and Henrici 1943, 339AL emend. Witt and Stackebrandt 1990, 370, emend. Wellington, Stackebrandt, Sanders, Wolstrup and Jorgensen, 1992, 159. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo M, Suzuki KE, Ludwig W, Whitman WB (eds) Bergey’s Manual of Systematic Bacteriology, 2nd edn, volume 5 Springer, USA (in press)

  • Kämpfer P, Kroppenstedt RM, Dott W (1991) A numerical classification of the genera Streptomyces and Streptoverticillium using miniaturized physiological tests. J Gen Microbiol 137:1831–1891

    Google Scholar 

  • Kim D, Chun J, Sahin N, Hah YC, Goodfellow M (1996) Analysis of thermophilic clades within the genus Streptomyces by 16S ribosomal DNA sequence comparisons. Int J Syst Bacteriol 46:581–587

    Article  CAS  Google Scholar 

  • Kim SB, Lonsdale JT, Seong C-N, Goodfellow M (2003) Streptacidiphilus gen. nov., a home for acidiphilic actinomycetes with a wall chemotype 1 and emendation of the family Streptomycetaceae (Waksman & Henrici 1943 emend Rainey et al. 1997) Antonie van Leeuwenhoek 83:107–116

  • Krainsky A (1914) Die Aktinomyceten und ihren Bedeutung in der Natur. Zentrlbl Bakteriol Parasiterikd Infektionkr Hyg II Abt 41:649–688

    Google Scholar 

  • Kumar Y, Goodfellow M (2008) Five new members of the Streptomyces violaceusniger 16S rRNA gene clade: Streptomyces castelarensis comb. nov., S. himastatinicus sp. nov., S. mordarskii sp. nov., S. rapamycinicus sp. nov. and S. ruanii sp. nov. Int J Syst Evol Microbiol 58:1369–1378

    Article  PubMed  CAS  Google Scholar 

  • Kumar Y, Goodfellow M (2010) Reclassification of Streptomyces hygroscopicus strains as Streptomyces aldersoniae sp. nov., Streptomyces augustmyceticus sp. nov., comb. nov., Streptomyces ascomycinicus sp. nov. Streptomyces decoyicus sp. nov., comb. nov., Streptomyces milbemycinicus sp. nov. and Streptomyces wellingtoniae sp. nov. Int J Syst Evol Microbiol 60:769–775

    Article  PubMed  Google Scholar 

  • Küster E (1959) Outline of a comparative study of criteria used in characterization of the actinomycetes. Int Bull Bacteriol Nomencl Taxon 9:97–104

    Article  Google Scholar 

  • Labeda DP (1992) DNA:DNA hybridization in the systematics of Streptomyces. Gene 115:249–253

    Article  PubMed  CAS  Google Scholar 

  • Labeda DP (1993) DNA:DNA relatedness among strains of the Streptomyces lavendulae phenotypic cluster group. Int J Syst Evol Microbiol 53:822–825

    Google Scholar 

  • Labeda DP (1998) DNA:DNA relatedness among the Streptomyces fulvissimus and Streptomyces griseoviridis phenotypic cluster groups. Int J Syst Evol Microbiol 48:829–832

    CAS  Google Scholar 

  • Labeda DP (2011) Multilocus sequence analysis of phytopathogenic Streptomyces species. Int J Syst Evol Microbiol 61:2379–2383

    Article  Google Scholar 

  • Labeda D, Kroppenstedt RM (2000) Phylogenetic analysis of Saccharothrix and related taxa: proposal for Actinosynnemataceae fam. nov. Int J Syst Evol Microbiol 50:331–336

    Article  PubMed  CAS  Google Scholar 

  • Labeda DP, Lyons AJ (1991a) Deoxyribonucleic acid relatedness among species of the “Streptomyces cyaneus” cluster. Syst Appl Microbiol 14:158–164

    Google Scholar 

  • Labeda DP, Lyons AJ (1991b) The Streptomyces violaceusniger cluster is heterogeneous in DNA relatedness among strains: emendation of the descriptions of S. violaceusniger and Streptomyces hygroscopicus. Int J Syst Bacteriol 41:398–401

    Article  Google Scholar 

  • Labeda DP, Price NP, Kroppenstedt RM, Donahue JM, Williams NM, Sells SF (2009) Streptomyces atriruber sp. nov. and Streptomyces silaceus sp. nov., two novel species of equine origin. Int J Syst Evol Microbiol 59:2899–2903

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Liu Z, Wang L, Zhang Y, Qi W, Goodfellow M (2001) Saccharopolyspora flava sp. nov. and Saccharopolyspora thermophila sp. nov., novel actinomycetes from soil. Int J Syst Evol Microbiol 51:319–325

    PubMed  CAS  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Buchner A, Yadhukumar Lai, Steppi S et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Manchester L, Pot B, Kersters K, Goodfellow M (1990) Classification of Streptomyces and Streptoverticillium species by numerical analysis of electrophoretic protein patters. Syst Appl Microbiol 13:333–337

    Google Scholar 

  • Mordarski M, Goodfellow M, Williams ST, Sneath PHA (1986) Evaluation of species groups in the genus Streptomyces. In: Szabó G, Biró S, Goodfellow M (eds) Biological, biochemical and biomedical aspects of actinomycetes. Akademiai Kiadó, Budapest, pp 517–525

    Google Scholar 

  • Ōmura S, Takahashi Y, Iwai Y, Tamaka H (1982) Kitasatosporia, a new genus of the order Actinomycetales. J Antibiot 35:1013–1019

    PubMed  Google Scholar 

  • Park MS, Jung SR, Lee MS, Kim KO, Do JO, Lee KH, Kim SB, Bae KS (2005) Isolation and characterization of bacteria associated with two sand dune plant species, Calystegia soldanella and Elymus mollis. J Microbiol 43:219–227

    PubMed  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, 8th edn edn. Williams and Wilkins Company, Baltimore, pp 748–829

    Google Scholar 

  • Ridell M, Wallerstrom G, Williams ST (1986) Immunodiffusion analysis of phenetically defined strains of Streptomyces, Streptoverticillium and Nocardiopsis. Syst Appl Microbiol 8:24–27

    Article  Google Scholar 

  • Rong X, Huang Y (2010) Taxonomic evaluation of the Streptomyces griseus clade using mulitilocus sequence analysis and DNA–DNA hybridization, with proposal to combine 29 species and three subspecies as 11 genomic species. Int J Syst Evol Microbiol 60:696–703

    Article  PubMed  CAS  Google Scholar 

  • Rong X, Gou Y, Huang Y (2009) Proposal to reclassify the Streptomyces albidoflavus clade based on the basis of multilocus sequence analysis and DNA–DNA hybridization, and taxonomic elucidation of Streptomyces griseus subsp solvifaciens. Syst Appl Microbiol 32:314–322

    Article  PubMed  CAS  Google Scholar 

  • Saddler GS, O’Donnell AG, Goodfellow M, Minnikin DE (1987) SIMCA pattern recognition in the analysis of streptomycete fatty acids. J Gen Microbiol 133:1137–1147

    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 

  • Schatz A, Bugie E, Waksman SA (1944) Streptomycin, a substance inhibiting antibiotic activity against gram-positive and gram-negative bacteria. Proc Soc Exp Biol Med 55:66–69

    CAS  Google Scholar 

  • Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Shirling EB, Gottlieb D (1968a) Cooperative description of type cultures of Streptomyces. II. Species descriptions from first study. Int J Syst Bacteriol 38:69–189

    Article  Google Scholar 

  • Shirling EB, Gottlieb D (1968b) Cooperative description of type cultures of Streptomyces. III. Additional species descriptions from first and second studies. Int J Syst Bacteriol 18:279–292

    Article  Google Scholar 

  • Shirling EB, Gottlieb (1969) Cooperative description of type cultures of Streptomyces. IV. Species descriptions from the second, third and fourth studies. Int J Syst Bacteriol 19:391–512

    Article  Google Scholar 

  • Shirling EB, Gottlieb D (1972) Cooperative description of type strains of Streptomyces V. Additional descriptions. Int J Syst Bacteriol 22:265–394

    Article  Google Scholar 

  • Sneath PHA (1970) Application of numerical taxonomy to Actinomycetales: problems and perspectives. In: Prauser H (ed) The Actinomycetales. Gustav Fischer, Jena, pp 371–378

    Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today Nov 06:152–155

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Tamura T, Ishida Y, Otoguro M, Hatano K, Suzuki K (2008a) Classification of ‘Streptomyces tenebrarius’ Higgins and Kastner as Streptoalloteichus tenebrarius nom. rev., comb. nov., and emended description of the genus Streptoalloteichus. Int J Syst Evol Microbiol 58:688–691

    Article  PubMed  CAS  Google Scholar 

  • Tamura T, Ishida Y, Otoguro M, Hatano K, Labeda D, Price NP, Suzuki K (2008b) Reclassification of Streptomyces caeruleus as a synonym of Actinoalloteichus cyanogriseus and reclassification of Streptomyces spheroides and Streptomyces laceyi as later synonyms of Streptomyces niveus. Int J Syst Evol Microbiol 58:2812–2813

    Article  PubMed  CAS  Google Scholar 

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

  • Trejo WH (1970) An evaluation of some concepts and criteria used in the speciation of streptomycetes. Trans NY Acad Sci Ser II 32:989–997

    Google Scholar 

  • Waksman SA (1919) Cultural studies of species of Actinomyces. Soil Sci 8:71–215

    Article  CAS  Google Scholar 

  • Waksman SA, Curtis RE (1916) The actinomycetes of the soil. Soil Sci 1:99–134

    Article  CAS  Google Scholar 

  • Waksman SA, Woodruff HB (1941) Actinomycetes antibioticus, a new soil organism antagonistic to pathogenic and non-pathogenic bacteria. J Bacteriol 42:231–249

    PubMed  CAS  Google Scholar 

  • Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ (1983) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743–1813

    PubMed  CAS  Google Scholar 

  • Williams ST, Goodfellow M, Alderson G (1989) Genus Streptomyces Waksman and Henrici 1943, 339AL. In: Williams ST, Sharpe ME, Holt JG (eds) Bergey’s manual of determinative bacteriology, volume 4. Williams and Wilkins, Baltimore, pp 2453–2492

    Google Scholar 

  • Witt D, Stackebrandt E (1990) Unification of the genera Streptoverticillium, Streptomyces, emendation of Streptomyces Waksman, Henrici 1943 339AL. Syst Appl Microbiol 13:361–371

    CAS  Google Scholar 

  • Xu C, Wang W, Cui Q, Huang Y, Liu Z, Zheng G, Goodfellow M (2006) Neutrotolerant acidiphilic Streptomyces species isolated from acidic-soils in China: Streptomyces guanduensis sp. nov., Streptomyces paucisporeus sp. nov., Streptomyces rubidus sp. nov. and Streptomyces yanglinensis sp. nov. Int J Syst Evol Microbiol 56:1109–1115

    Article  PubMed  CAS  Google Scholar 

  • Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer K-H, Ludwig W, Glöckner FO, Roselló-Móra R (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree for all sequenced type strains. Sys Appl Microbiol 31:241–250

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The able technical assistance of E. N. Hoekstra for isolation of genomic DNA and determination of the sequences is gratefully acknowledged. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. P. Labeda.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 49 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Labeda, D.P., Goodfellow, M., Brown, R. et al. Phylogenetic study of the species within the family Streptomycetaceae . Antonie van Leeuwenhoek 101, 73–104 (2012). https://doi.org/10.1007/s10482-011-9656-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-011-9656-0

Keywords

Navigation