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Biosystematics and diversity amongst novel carboxydotrophic actinomycetes

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Abstract

Fifty-four carboxydotrophic actinomycetes isolated from soils and composts were compared through 119 unit characters with representative mesophilic and thermophilic streptomycetes. The data were examined using the Jaccard, pattern and simple matching coefficients and clustering achieved using the unweighted pair group method with arithmetic averages algorithm. Acceptable cophenetic correlation and test error values allowed confidence to be placed in the resultant numerical taxonomies. The carboxydotrophic actinomycetes, which were distinct from cluster-groups corresponding to the mesophilic and thermophilic streptomycetes, formed two major cluster-groups the members of which were examined for the presence of diagnostic chemical markers. All but two of the carboxydotrophic actinomycetes had a profile of chemical properties consistent with their assignment to the genusStreptomyces. Quantitative fatty acid data were examined using the SIMCA package and the two statistically significant groups obtained corresponded with the cluster-groups circumscribed in the numerical phenetic analysis. Members of the two groups were also distinguished on the basis of their phospholipid composition. The two strains that containedmeso- as opposed to LL-diaminopimelic acid in their peptidoglycan also showed a distinct chemotaxonomic profile. It was concluded that the carboxydotrophic actinomycetes form a novel and taxonomically diverse group.

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References

  • Ambler RP (1985) Protein sequencing and taxonomy.In: Goodfellow M, Jones D & Priest FG (Eds) Computer-Assisted Bacterial Systematics (pp 307–335). Academic Press, London

    Google Scholar 

  • Barrow GI & Feltham RKA (1993) Cowan and Steel's Manual for the Identification of Medical Bacteria. Cambridge University Press, Cambridge

    Google Scholar 

  • Bates RG & Bower VE (1956) Alkaline solutions for pH control. Anal. Chem. 26: 1322–1324

    Google Scholar 

  • Bell JM, Williams E & Colby J (1985) Carbon monoxide oxidoreductases from thermophilic bacteria. In: Poole RK & Dow CS (Eds.) Microbial Gas Metabolism (pp 153–159). Academic Press, London

    Google Scholar 

  • Bell JM, Falconer C, Colby J & Williams E (1987) CO metabolism by a thermophilic actinomycete,Streptomyces strain G26. J. Gen. Microbiol. 133: 3445–3456

    Google Scholar 

  • Bell JM, Colby J & Williams E (1988) CO oxidoreductase fromStreptomyces G26 is a molybedenum hydroxylase. Biochem. J. 250: 605–612

    Google Scholar 

  • Blomquist G, Johansson E, Soderstrom B & Wold S (1979a) Classification of fungi by means of pyrolysis-gas chromatography pattern recognition. J. Chromat. 173: 19–32

    Google Scholar 

  • Blomquist G, Johansson E, Soderstrom G & Wold S (1979b) Reproducibility of pyrolysis-gas chromatographic analyses of the moldPenicillium brevi-compactum. J. Chromat. 173: 7–17

    Google Scholar 

  • Blomquist G, Johansson E, Soderstrom B & Wold S (1979c) Classification of fungi by means of pyrolysis gas chromatography pattern recognition. J. Chromat. 173: 19–32

    Google Scholar 

  • Colby J, Williams E & Turner APF (1985) Applications of CO utilising microorganisms. Trends in Biotechnology 3: 12–17

    Google Scholar 

  • Colwell RR (1970) Polyphasic taxonomy of bacteria. In: Iizuka H & Hasegawa T (Eds) Culture Collections of Microorganisms (pp 421–436). University of Tokyo Press, Tokyo

    Google Scholar 

  • Colwell RR (1973) Genetic and phenotypic classification of bacteria. Adv. Appl. Microbiol. 16: 137–175

    Google Scholar 

  • Embley TM, Smida J & Stackebrandt E (1988) The phylogeny of mycolateless wall chemotype IV actinomycetes and description ofPseudonocardiaceae fam. nov. System. Appl. Microbiol. 11: 44–52

    Google Scholar 

  • Falconer C, Goodfellow M. O'Donnell AG & Williams E (1993) The isolation of carbon monoxide utilising actinomycetes from soils. FEMS Ecol. Lett. submitted

  • Frazier NC (1926) A method for the detection of changes in gelatin due to bacteria. J. Infec. Dis. 39: 302–309

    Google Scholar 

  • Frunzke K & Meyer O (1990) Nitrate respiration, denitrification and utilisation of nitrogen sources by aerobic carbon monoxide-oxidising bacteria. Arch. Microbiol. 154: 168–174

    Google Scholar 

  • Gadkari D, Schricker K, Acker G, Kroppenstedt & Meyer O (1990)Streptomyces thermoautotrophicus sp. nov., a thermophilic CO-oxidizing and H2-oxidizing obligate chemolithoautotroph. Appl. Environ. Microbiol. 56: 3727–3734

    Google Scholar 

  • Gadkari D, Morsdorf G, & Meyer O (1992) Chemolithoautotrophic assimilation of dinitrogen byStreptomyces thermoautotrophicus ubt 7. Identification of an unusual N2-fixing system. J. Bacteriol. 174: 6840–6843

    Google Scholar 

  • Goodfellow M. (1989) Suprageneric classification of actinomycetes. In: Williams ST, Sharpe ME & Holt JG (Eds) Bergey's Manual of Systematic Bacteriology, Volume 4 (pp 2333–2339). Williams & Wilkins, Baltimore

    Google Scholar 

  • Goodfellow M, Alderson G & Lacey J (1979) Numerical taxonomy ofActinomadura and related actinomycetes. J. Gen. Microbiol. 112: 95–111

    Google Scholar 

  • Goodfellow M, Mordarski M, Tkacz A, Szyba K & Pulverer G (1980) Polynucleotide sequence divergence among some coagulase-negative staphylococci. Zentbl. Bakt. ParasitKde (Abt 1) A246; 10–22

    Google Scholar 

  • Goodfellow M, Lonsdale C, James AL & MacNamara OC (1987a) Rapid biochemical tests for the characterisation of streptomycetes. FEMS Microbiol. Lett. 43: 39–44

    Google Scholar 

  • Goodfellow M, Lacey J & Todd C (1987b) Numerical classification of thermophilic streptomycetes. J. Gen. Microbiol. 133: 3135–3149

    Google Scholar 

  • Goodfellow M, Stanton LJ, Simpson KE & Minnikin DE (1990) Numerical and chemical classification ofActinoplanes and some related actinomycetes. J. Gen. Microbiol. 13: 19–36

    Google Scholar 

  • Gordon RE (1968) The taxonomy of soil bacteria. In: Gray TRG & Parkinson D (Eds) The Ecology of Soil Bacteria. (pp. 293–321): Liverpool University Press, Liverpool

    Google Scholar 

  • Gordon RE & Mihm JM (1962) Identification ofNocardia caviae (Erikson) nov. comb. Ann. N.Y. Aca. Sci. 98: 628–639

    Google Scholar 

  • Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53: 325–338

    Google Scholar 

  • Hugendieck I & Meyer O (1992) The structural genes encoding CO dehydrogenase subunits (cox 1, m and s) inPseudomonas carboxydovorans on 5 reside on plasmid phcg 3 and are, with the exception ofStreptomyces thermoautotrophicus, conserved in carboxydotrophic bacteria. Arch. Microbiol. 157: 301–304

    Google Scholar 

  • Izard D, Gavini F & Leclerc H (1980) Polynucleotide sequence relatedness and genome size amongEnterobacter intermedium sp. nov. and the speciesEnterobacter cloacae andKlebsiella pneumoniae. Zentbl. Bakt. ParasitKde (Abt 1) Cl: 51–60

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

    Google Scholar 

  • Lechevalier MP & Lechevalier HA (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int. J. Syst. Bacteriol. 20: 435–443

    Google Scholar 

  • Lyons CM, Justin P, Colby C & Williams E (1984) Isolation, characterisation and autotrophic metabolism of a moderately thermophilic carboxydobacterium,Pseudomonas thermocarboxydovorans sp. nov. J. Gen. Microbiol. 130: 1097–1105

    Google Scholar 

  • Küster E & Williams ST (1964) Production of hydrogen sulphide by streptomycetes and methods for its detection. Appl. Microbiol. 12: 46–52

    Google Scholar 

  • McIlvaine TC (1921) A buffer solution for colorimetric comparison. J. Biol. Chem. 49: 183–186

    Google Scholar 

  • Meyer O & Schlegel HG (1983) Biology of aerobic carbon monoxide utilising bacteria. Ann. Rev. Microbiol. 37: 277–310

    Google Scholar 

  • Meyer O, Frunzke K, Gadkari D, Jacobitz S, Hugendieck I & Kraut M (1990) Utilisation of carbon monoxide by aerobes-Recent advances. FEMS Microbiol. Rev. 87: 253–260

    Google Scholar 

  • Meyer O, Frunzke K & Morsdorf G (1993) Biochemistry of the aerobic utilization of carbon monoxide. In: Murrell JC & Kelly DP (Eds.) Microbial Growth on C1 Compounds (pp 433–459). Intercept Scientific Ltd., Andover

    Google Scholar 

  • Minnikin DE, Hutchinson IG, Caldicott AB & Goodfellow M (1980) Thin-layer chromatography of methanolysates of mycolic acid-containing bacteria. J. Chromat. 188: 221–233

    Google Scholar 

  • Minnikin DE, O'Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A & Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J. Microbiol. Meth 2: 233–241

    Google Scholar 

  • Mordarska H, Mordarski M & Goodfellow M (1972) Chemotaxonomic characters and classification of some nocardioform bacteria. J. Gen. Microbiol. 71: 77–86

    Google Scholar 

  • O'Donnell AG (1985) Numerical analysis of chemotaxonomic data.In: Goodfellow M, Jones D & Priest FG (Eds) Computer-Assisted Bacterial Systematics (pp 403–415). Academic Press, London

    Google Scholar 

  • O'Donnell AG (1988a) Recognition of novel actinomycetes.In: Goodfellow M, Williams ST & Mordarski M (Eds.) Actinomycetes inBiotechnology (pp 69–88). Academic Press, London

    Google Scholar 

  • O'Donnell AG (1988b) Assessment of taxonomic congruence using multivariate statistical techniques.In: Okami Y, Beppu T & Ogawara H (Eds) Biology of Actinomycetes '88 (pp 257–262). Japan Scientific Societies Press, Tokyo

    Google Scholar 

  • O'Donnell AG (1988c) Numerical analysis of chemotaxonomic data.In: Goodfellow M, Jones D & Priest FG (Eds) Computer-Assisted Bacterial Systematics (pp 403–431). Academic Press, London

    Google Scholar 

  • O'Donnell AG, Goodfellow M & Minnikin DE (1982) Lipids in the classification ofNocardioides: Reclassification ofArthrobacter simplex (Jensen) Lochhead in the genusNocardioides (Prauser) emend. O'Donnell et al. asNocardioides simplex comb. nov. Arch. Microbiol. 133: 323–329

    Google Scholar 

  • O'Donnell AG, Nahaie MR, Goodfellow M, Minnikin DE & Hájek V (1985) Numerical analysis of fatty acid profiles in the identification of staphylococci. J. Gen. Microbiol. 131: 2023–2033

    Google Scholar 

  • O'Donnell AG, MacFie HJH & Norris JR (1988) An assessment of taxonomic congruence between DNA-DNA hybridization and pyrolysis gas-liquid chromatographic classifications. J. Gen. Microbiol. 134: 743–749

    Google Scholar 

  • O'Donnell AG, Embley TM & Goodfellow M (1993) Future of bacterial systematics. In Goodfellow M & O'Donnell AG (Eds) Handbook of New Bacterial Systematics (pp 513–524) Academic Press, London

    Google Scholar 

  • Pridham TG, Hesseltine CW & Benedict RG (1958) A guide for the classification of streptomycetes according to selected groups. Placement of strains in morphological sections. Appl. Microbiol. 6: 52–79

    Google Scholar 

  • Saddler GS, Goodfellow M, Minnikin DE & O'Donnell AG (1986) Influence of the growth cycle on the fatty acid and menaquinone composition ofStreptomyces cyaneus NCIB 9616. J. Appl. Bacteriol. 60: 51–56

    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

    Google Scholar 

  • Shirling EB & Gottlieb D (1966) Methods for the characterisation ofStreptomyces species. Int. J. System. Bacteriol. 16: 313–340

    Google Scholar 

  • Slifkin M & Gil GM (1983) Rapid biochemical tests for the identification of groups A,B,C,F, and G streptococci from throat cultures. J. Clin. Microbiol. 18: 29–32

    Google Scholar 

  • Skerman VBD (1967) A Guide to the Identification of the Genera of Bacteria, 2nd Edition. Williams and Wilkins, Baltimore

    Google Scholar 

  • Sneath PHA (1957) The application of computers to taxonomy. J. Gen. Microbiol. 17: 201–226

    Google Scholar 

  • Sneath PHA (1968) Vigour and pattern in taxonomy. J. Gen. Microbiol. 54: 1–11

    Google Scholar 

  • Sneath PHA (1985) Future of numerical taxonomy.In: Goodfellow M, Jones D & Priest FG (Eds) Computer-Assisted Bacterial Systematics (pp 415–431), Academic Press, London

    Google Scholar 

  • Sneath PHA & Johnson R (1972) The influence on numerical taxonomic similarities of errors in microbiological tests. J. Gen. Microbiol. 72: 377–392

    Google Scholar 

  • Sneath PHA & Sokal RR (1973) Numerical Taxonomy. The Principles and Practice of Numerical Classification. W.H. Freeman, San Francisco

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Suzuki K, Goodfellow M & O'Donnell AG (1993) Cell envelopes and classification.In: Goodfellow M & O'Donnell AG (Eds) Handbook of New Bacterial Systematics (pp 195–250). Academic Press, London

    Google Scholar 

  • Tresner HD, Davies MC & Backus EJ (1961) Electron microscopy ofStreptomyces spore morphology and its role in species differentiation. J. Bacteriol. 81: 70–80

    Google Scholar 

  • Wellington EMH & Williams ST (1978) Preservation of actinomycete inoculum in frozen glycerol. Microbios Lett. 6: 151–157

    Google Scholar 

  • Williams R, Colby J, Lyons CM & Bell J (1986) The bacterial utilisation of synthetic gases containing carbon monoxide. Biotech. Gen. Eng. Rev. 4: 169–211

    Google Scholar 

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

    Google Scholar 

  • Williams ST, Goodfellow M & Alderson G (1989) GenusStreptomyces Waksman and Henrici 1943, 339AL.In: Williams ST, Sharpe ME & Holt JG (Eds) Bergey's Manual of Systematic Bacteriology, Volume 4 (pp 2452–2492). Williams & Wilkins, Baltimore

    Google Scholar 

  • Wishart D (1978) Clustan User Manual. Version IC, Release 2, 3rd edn, Edinburgh University Program Library Unit, Edinburgh

    Google Scholar 

  • Wold S (1976) Pattern recognition by means of disjoint principal components models. Pattern Recognition 8: 127–139

    Google Scholar 

  • Wold S (1978) Cross-validatory estimation of the number of components in factor and principal components models. Technometrics 20: 397–405

    Google Scholar 

  • Wold S & Sjøstrom MJ (1977) SIMCA: A method for analysing chemical data in terms of similarity and analogy.In: Kowalski B (Ed) Chemometrics: Theory and Application (pp 243–282). American Chemical Society, ACS Symposium Series no 52, Washington DC

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Authors and Affiliations

  1. Department of Agricultural and Environmental Science, The University, NEI 7RU, Newcastle upon Tyne, UK

    Anthony G. O'Donnell

  2. Department of Microbiology, The University, NEI 7RU, Newcastle upon Tyne, UK

    Christine Falconer, Michael Goodfellow, Alan C. Ward & Edwin Williams

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  1. Anthony G. O'Donnell
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  2. Christine Falconer
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  3. Michael Goodfellow
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O'Donnell, A.G., Falconer, C., Goodfellow, M. et al. Biosystematics and diversity amongst novel carboxydotrophic actinomycetes. Antonie van Leeuwenhoek 64, 325–340 (1993). https://doi.org/10.1007/BF00873091

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