Abstract
Members of three putatively novel Streptomyces species, designated Streptomyces groups A, B and C, were repeatedly isolated from environmental samples taken from four hay meadow plots at Cockle Park Experimental Farm, Northumberland (UK). Representative isolates were found to have properties consistent with their classification in the genus Streptomyces and were recovered in three taxa using different phenotypic criteria, namely morphological and pigmentation properties, rapid enzyme tests, and whole-organism fatty acid, protein electrophoretic and pyrolysis mass-spectrometric data. The isolates were rapidly characterised as three taxonomic groups using pyrolysis mass spectrometry. The three taxa were also distinguished from one another and from validly described species of Streptomyces using rapid enzyme tests based on the fluorophores 7-amino-methylcoumarin and 4-methylumbelliferone, and computer-assisted identification procedures. The results indicate that selective isolation and rapid characterisation of streptomycetes using pyrolysis mass spectrometry provide a practical way of determining the phenotypic species diversity of streptomycetes in natural habitats. The experimental data also indicate that representative sampling of cultivable streptomycetes from soil can best be achieved using a multi-step extraction procedure coupled with the use of selective isolation procedures.
Similar content being viewed by others
References
Bull AT, Goodfellow M & Ward AC (2000) Search and discovery strategies for biotechnology: the paradigm shift. Microbiol. Mol. Biol. Rev. 64 (in press)
Chun J, Atalan E, Kim S-B, Kim H-J, Hamid ME, Trujillo ME, Magee JG, Manfio GP, Ward AC & Goodfellow M (1993a) Rapid identification of streptomycetes by artificial neural network analysis of pyrolysis mass spectra. FEMS Microbiol. Lett. 114: 115–120
Chun J, Atalan E, Ward AC & Goodfellow M (1993b) Artificial neural network analysis of pyrolysis mass spectrometric data in the identification of Streptomyces strains. FEMS Microbiol. Lett. 107: 321–326
Colquhoun JA, Heald SC, Li L, Tamaoka J, Kato C, Horikoshi K & Bull AT (1998a) Taxonomy and biotransformation activities of some deep-sea actinomycetes. Extremophiles 2: 269–277
Colquhoun JA, Mexson J, Goodfellow M, Ward AC, Horikoshi K & Bull AT (1998b) Novel rhodococci and other mycolate actinomycetes from the deep sea. Antonie van Leeuwenhoek74: 27–40
Colquhoun JA, Zulu J, Goodfellow M, Horikoshi K, Ward AC & Bull AT (2000) Rapid characterisation of deep-sea actinomycetes for biotechnology screening programmes. Antonie van Leeuwenhoek (in press)
Embley TM & Stackebrandt E (1997) Species in practice: exploring uncultured prokaryote diversity in national samples. In: Claridge MF, Dawal HA & Wilson MR (Eds) Species: the Units of Biodiversity (pp. 61–81). Chapman & Hall, London
Ferguson EV, Ward AC, Sanglier J-J & Goodfellow M (1996) Evaluation of Streptomyces species-groups by pyrolysis mass spectrometry. Zbl. Bakt. 285: 169–181
Goodfellow M & Haynes JA (1984) Actinomycetes in marine sediments. In: Ortiz-Ortiz L, Bojalil LF & Yakoleff V (Eds) Biological, Biochemical and Biomedical Aspects of Actinomycetes (pp. 452–472). Academic Press, Orlando
Goodfellow M, Lonsdale C, James AL & MacNamara OC (1987a) Rapid biochemical tests for the characterisation of streptomycetes. FEMS Microbiol. Lett. 43: 39–44
Goodfellow M, Ferguson EV & Sanglier J-J (1992) Numerical classification and identification of Streptomyces species-a review. Gene 115: 225–233
Goodfellow M, Davenport R, Stainsby SM & Curtis TP (1996) Actinomycete diversity associated with foaming in activated sludge plants. J. Ind. Microbiol. 17: 268–280
Hamid ME, Chun J, Magee JG, Minnikin DE & Goodfellow M (1994) Rapid characterisation and identification of mycobacteria using fluorogenic enzyme tests. Zbl. Bakt. 280: 476–487
Hattori T & Hattori R (1976) The physical environment in soil microbiology: an attempt to extend principles of microbiology to soil microorganisms. CRC Crit Rev Microbiol4: 423–461
Hopkins DW, MacNaughton SJ & O'Donnell AG (1991a) A dispersion and differential centrifugation technique for representatively sampling microorganisms from soil. Soil Biol. Biochem. 23: 217–225
Hopkins DW, O'Donnell AG & MacNaughton SJ (1991b) Evaluation of a dispersion and elutriation technique for sampling microorganisms from soil. Soil Biol. Biochem. 23: 227–232
Hsu SC & Lockwood JL (1975) Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl. Microbiol. 29: 422–426
Jones KL (1949) Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J. Bacteriol. 57: 141–145
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
Kay HE, Coutinho HLC, Fattori M, Manfio GP, Goodacre R, Nuti MP, Basaglia M. & Beringer JE (1994) The identification of Bradyrhizobium japonicum strains isolated from Italian soils. Microbiology 140: 2333–2339
Kelly KL (1958) Centroid notations for the revised ISCC-NBS color name blocks. J. Res. Nat. Bureau Standards USA 61: 427
Kim B, Sahin N, Minnikin DE, Zakrzewska-Czerwinska J, Mordarski M & Goodfellow M (1999) Classification of thermophilic actinomycetes, including the description of Streptomyces thermoalcalitolerans sp. nov. Int. J. Syst. Bacteriol. 49: 7–17
Kroppenstedt RM, Stackebrandt E & Goodfellow M (1990) Taxonomic revision of the actinomycete genera Actinomadura and Microtetraspora. System Appl. Microbiol. 13: 148–160
Küster E (1959) Outline of a comparative study of criteria used in characterization of the actinomycetes. Int. Bull. Bacteriol. Nomencl. Taxon.9: 97–104
Küster E & Williams ST (1964) Selection of media for isolation of streptomycetes. Nature 202: 928–929
Labeda DP (1993) DNA relatedness among strains of the Streptomyces lavendulae phenotypic cluster group. Int. J. Syst. Bacteriol. 43: 822–825
Labeda DP (1996) DNA relatedness among verticil-forming Streptomyces species (formerly Streptoverticillium species). Int. J. Syst. Bacteriol. 46: 699–703
Labeda DP (1999) DNA relatedness among the Streptomyces fulvissimus and Streptomyces griseovirdis phenetic cluster groups. Int. J. Syst. Bacteriol. 48: 829–832
Labeda DP & Lyons AJ (1991a) Deoxyribonucleic acid relatedness among species of the Streptomyces cyaneus cluster. Syst. Appl. Microbiol. 14: 158–164
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
Labeda DP, Lechevalier MP & Testa RT (1997) Streptomyces stramineus sp. nov., a new species of the verticillate streptomycetes. Int. J. Syst. Bacteriol. 47: 747–753
Langham CD, Williams ST, Sneath PHA & Mortimer AM (1989) New probability matrices for identification of Streptomyces. J. Gen. Microbiol. 135: 121–133
MacDonald RM (1986) Sampling soil microfloras: dispersion of soil by ion exchange and extraction of specific microorganisms by elutriation. Soil Biol. Biochem. 18: 399–406
MacNaughton SJ & O'Donnell AG (1994) Tuberculostearic acid as a means of estimating the recovery (using dispersion and differential centrifugation) of actinomycetes from soil. J. Microbiol. Meth. 20: 69–77
Manchester L, Pot B, Kersters K & Goodfellow M (1990) Classi-fication of Streptomyces and Streptoverticillium species by numerical analysis of electrophoretic protein patterns. Syst. Appl. Microbiol. 13: 333–337
Manfio GP (1995) Towards Minimal Standards for the Description of Streptomyces species. Ph.D. thesis, University of Newcastle upon Tyne, UK
Manfio GP, Zakrzewska-Czerwinska J, Atalan E & Goodfellow M (1995) Towards minimal standards for the description of Streptomyces species. In: Debabov VG, Dudnik YV & Danilenko VN (Eds) The Biology of the Actinomycetes '94: Proceedings of the Ninth International Symposium on the Biology of the Actinomycetes (pp. 242–252). All-Russia Scientific Research Institute for Genetics and Selection of Industrial Microorganisms, Moscow
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, vol. B (pp. 517–525). Akadémiai Kiadó, Budapest
Muyzer G & Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73: 127–141
National Bureau of Standards (1964) ISCC-NBS Color-name Charts Illustrated with Centroid Colors (Supplement to National Bureau of Standards USA circular 553). National Bureau of Standards, USA
Niepold F, Conrad R & Schlegel HG (1979) Evaluation of the ef-ficiency of extraction for quantitative estimation of hydrogen bacteria in soil. Antonie van Leeuwenhoek 45: 485–497
Nishiyama M, Senoo K, Wada H & Matsumato S (1992) Identi-fication of soil micro-habitats for growth, death and survival of a bacterium,-1,2,3,4,5,6,-hexachlorocyclohexane-assimilating Sphingomonas paucimobilis, by fractionation of soil. FEMS Microbiol. Ecol. 101: 145–150
Ochi K (1995) A taxonomic study of the genus Streptomyces by analysis of ribosomal protein AT-L30. Int. J. Syst. Bacteriol. 45: 507–514
O'Donnell AG, Falconer C, Goodfellow M, Ward AC & Williams E (1993) Biosystematics and diversity amongst novel carboxydotrophic actinomycetes. Antonie van Leeuwenhoek 64: 325–340
O'Sulliven DJ (1999) Methods of analysis of the intestinal micro-flora. In: Tannock GW (Ed) Probiotics a Critical Review (pp. 25–44). Horizon Scientific Press, Wymondham
Paradis E, Goyer C, Hodge NC, Hogue R, Stall RE & Beaulieu C (1994) Fatty acid and protein profiles of Streptomyces scabies strains isolated in eastern Canada. Int. J. Syst. Bacteriol. 44: 561–564
Pawson HC (1960) Cockle Park Farm. Oxford University Press, London
Pot B, Gillis M, Hoste B, Jan Den Velde A, Bekaert F, Kersters K & De Ley J (1989) Intrageneric and intergeneric relationships of the genus Oceanospirillum. Int. J. Syst. Bacteriol. 39: 23–34
Pridham TG & Lyons JR (1961) Streptomyces albus (Rossi Doria) Waksman et Henrici: taxonomic study of strains labelled Streptomyces albus. J. Bacteriol. 81: 431–441
Pridham TG, Anderson P, Foley C, Lindenfelser C, Hesseltine CW & Benedict RG (1956–1957) A selection of media for maintenance and taxonomic study of streptomycetes. Antibiotic Annual: 947–953
Ramsay AJ (1984) Extraction of bacteria from soil: efficiency of shaking or ultrasonication as indicated by direct counts and autoradiography. Soil Biol. Biochem. 16: 475–481
Sacks E & Alderton G (1961) Behaviour of bacterial spores in aqueous polymer two-phase systems. J. Bacteriol. 82: 331–341
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
Sanglier J-J, Whitehead D, Saddler GS, Ferguson EV & Goodfellow M(1992) Pyrolysis mass spectrometry as a method for the classi-fication, identification and selection of actinomycetes. Gene 115: 235–242
Shirling EB & Gottlieb D (1966) Methods for characterisation of Streptomyces species. Int. J. Syst. Bacteriol. 16: 313–340
Sneath PHA (1977) The maintenance of large numbers of strains of microorganisms and the implications for culture collections. FEMS Microbiol. Lett.1: 333–334
Sneath PHA (1979) BASIC program for identification of an unknown with presence-absence data against an identification matrix of percent positive characters. Comput. Geosc.5: 195–213
Sneath PHA & Johnson R (1972) The influence on numerical taxonomic similarities of errors in microbiological tests.J. Gen. Microbiol. 72: 377–392
Sneath PHA & Sokal RR (1973) Numerical Taxonomy: the Principles and Practice of Numerical Classification. W. H. Freeman, Baltimore
Sokal RR & Michener CD (1958) A statistical method for evaluating systematic relationships. Kansas Univ. Sci. Bull. 38: 1409–1438
Staneck JL & Roberts GD (1974) Simplified approach to identi-fication of aerobic actinomycetes by thin-layer chromatography. Appl. Microbiol. 28: 226–231
Sveshnikova MA, Chormonova NT, Lavrova NV, Terekhova LP & Preobrazhenskaya TP (1976) Isolation of soil actinomycetes on selective media with novobiocin (in Russian). Antibiotiki 21: 784–787
Tannock GW (1999) Analysis of the intestinal microflora: a renaissance. Antonie van Leeuwenhoek76: 265–278
Thompson CJ, Ward JM & Hopwood DA (1980) DNA cloning in Streptomyces: resistance genes from antibiotic-producing species. Nature 286: 525–527
Torsvik V, Goksoyr J & Daale FL (1990) High diversity in DNA of soil bacteria. Appl. Environ. Microbiol.56: 782–787
Trujillo M & Goodfellow M (1997) Polyphasic taxonomic study of clinically significant actinomadurae including the description of Actinomadura latina sp. nov. Zbl. Bakt. 285: 212–233
Vickers JC & Williams ST (1987) An assessment of plate inoculation procedures for the enumeration and isolation of soil streptomycetes. Microbios. Lett.35: 113–117
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 (pp. 553–561. Academic Press, London
Ward DM, Weller R & Bateson M (1990) 16S rRNA sequences reveal numerous uncultivated micro-organisms in natural environments. Nature 345: 63–65
Wishart D (1978) CLUSTAN user manual Version 1C, Release 2, 3rd edn. Edinburgh University Program Library Unit, Edinburgh
White DC (1983) Analysis of microorganisms in terms of quantity and activity in natural environments. In: Slater JH, Whittenbury R & Wimpenny JWT (Eds) Microbes in their Natural Environments (pp. 37–66). Cambridge University Press, Cambridge
Williams ST & Vickers JC (1988) Detection of actinomycetes in a natural environment-problems and perspectives. In: Okami Y, Beppu T & Ogawara H (Eds) Biology of Actinomycetes '88 (pp. 265–270). Japan Scientific Societies Press, Tokyo
Williams ST, Sharples GP & Bradshaw RM (1973) The fine structure of the Actinomycetales. In: Sykes G & FA Skinner (Eds) Actinomycetales: Characteristics and Practical Importance (pp. 113–130). Academic Press, London
Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA & Sackin MJ (1983a) Numerical classification of Streptomyces and related genera. J. Gen. Microbiol. 129: 1743–1813
Williams ST, Goodfellow M, Wellington EMH, Vickers JC, Alderson G, Sneath PHA, Sackin MJ & Mortimer AM (1983b) A probability matrix for identification of some streptomycetes. J. Gen. Microbiol. 129: 1815–1830
Williams ST, Goodfellow M & Vickers JC (1984) New microbes from old habitats? In: Kelly DP & Carr G (Eds) The Microbe II: Prokaryotes and Eukaryotes (pp. 219–256). Cambridge University Press, Cambridge
Williams ST, Vickers JC & Goodfellow M (1985) Application of new theoretical concepts to the identification of streptomycetes. In: Goodfellow M, Jones D & Priest FG (Eds) Computer-Assisted Bacterial Systematics (pp. 289–306). Academic Press, London
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 Systematic Bacteriology, vol. 4 (pp. 2452–2492). Williams & Wilkins, Baltimore
Witt D & Stackebrandt E (1990) Unification of the genera Streptoverticillium and Streptomyces, and emendation of Streptomyces Waksman and Henrici 1943, 339AL. Syst. Appl. Microbiol. 13: 361–371
Zakrzewska-Czerwinska J, Mordarski M & Goodfellow M (1988) DNA base composition and homology values in the classification of some Rhodococcus species. J. Gen. Microbiol. 134: 2807–2813
Zelles L & Bai QY (1994) Fatty acid patterns of phospholipids and lipopolysaccharides in environmental samples. Chemosphere 28: 391–411
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Atalan, E., Manfio, G.P., Ward, A.C. et al. Biosystematic studies on novel streptomycetes from soil. Antonie Van Leeuwenhoek 77, 337–353 (2000). https://doi.org/10.1023/A:1002682728517
Issue Date:
DOI: https://doi.org/10.1023/A:1002682728517