Abstract
Large numbers of putatively novel streptomycetes were isolated from rhizosphere soils of Albizia distachya, Colutea arborescens, Gleditsia triancanthos, Medicago arborea, Robinia pseudoacacia, Sophora japonica, Spartium junceum, Tipuana tipu and Wisteria sinensis. Representative isolates were determined to 6 multi-membered and 11 single-membered colour groups based on their ability to form pigments on oatmeal and peptone yeast extract iron agars. The largest colour groups, which encompassed 40 isolates with morphological properties typical of members of the Streptomyces violaceusniger 16S rRNA gene clade, were tested for a characteristic PCR amplification product with taxon-specific primers. In spite of highest 16S rRNA gene nucleotide similarity among the isolated strains belonging to the S. violaceusniger 16S rRNA gene clade, it is evident from the phenotypic, molecular and chemical results obtained that many new species will emerge.
Similar content being viewed by others
References
Al-Tai A, Kim B, Kim SB, Manfio GP, Goodfellow M (1999) Streptomyces malaysiensis sp. nov., a new streptomycete species with rugose, ornamented spores. Int J Syst Bacteriol 49:1395–1402
Anderson AS, Wellington EMH (2001) The taxonomy of Streptomyces and related genera. Int J Syst Evol Microbiol 51:797–814
Atalan E, Manfio GP, Ward AC, Kroppenstedt RM, Goodfellow M (2000) Biosystematic studies on novel streptomycetes from soil. Antonie van Leeuwenhoek 77:337–353
Blaak H, Schnellmann J, Walter S, Henrissat B, Schrempf H (1993) Characteristics of an exochitinase from Streptomyces olivaceoviridis, its corresponding gene, putative protein domainsand relationship to other chitinases. Eur J Biochem 214:659–669
Chamberlain K, Crawford DL (1999) In vitro and in vivo antagonism of pathogenic turfgrass fungi by Streptomyces hygroscopicus strains YCED 9 and WYE 53. J Ind Microbiol Biotechnol 23:641–646
Chun J (1995) Computer assisted classification and identification of actinomycetes. PhD thesis, Department of Microbiology, University of Newcastle, Newcastle upon Tyne, UK
Chun J, Goodfellow M (1995) A phylogenetic analysis of the genus Nocardia with 16 S rRNA gene sequences. Int J Syst Bacteriol 45:240–245
Conn VM, Franco CMM (2004) Analysis of the endophytic actinobacterial population in roots of wheat (Triticum aestivum L.) by terminal restriction fragments length polymorphism and sequencing of 16 S rRNA Clones. Appl Environ Microbiol 70:1787–1794
Coombs JT, Franco CMM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608
Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905
Doumbou CL, Salove MKH, Crawford DL, Beaulieu C (2002) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytology 82:85–102
Duangmal K, Ward AC, Goodfellow M (2005) Selective isolation of members of the Streptomyces violaceoruber clade from soil. FEMS Microbiol Lett 245:321–327
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1993) PHYLIP (Phylogenetic Inference Package), version 3.5c. Department of Genetics, University of Washington, Seattle
Getha K, Vikineswary S (2002) Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f.sp. cubense race 4: indirect evidence for the role of antibiosis in the antagonistic process. J Ind Microbiol Biotechnol 28:303–310
Goodfellow M, Ferguson EV, Sanglier JJ (1992) Numerical classification and identification of Streptomyces species: a review. Gene 115:225–233
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
Gupta R, Saxena RK, Chaturvedi P, Virdi JS (1995) Chitinase production by Streptomyces viridificans: its potential in fungal cell wall lysis. J Appl Bacteriol 78:378–383
Harchand RK, Singh S (1997) Extracellular cellulose system of a thermotolerant Streptomycete: Streptomyces albaduncus. Acta Microbiolica Immunol Hunganca 44(3):229–239
Hayakawa M, Yoshida Y, Iimura Y (2004) Selective isolation of bioactive soil actinomycetes belonging to the Streptomyces violaceusniger phenotypic cluster. J Appl Microbiol 96:973–981
Ilic SB, Konstantinovic SS, Todorovic ZB, Lazic ML, Veljkovic VB, Jokovic N, Radovanovic BC (2007) Characterization and antimicrobial activity of the bioactive metabolites in streptomycete isolates. Microbiology 76:421–428
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic, New York, pp 21–132
Kämpfer P, Kroppenstedt RM (1996) Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42:989–1005
Kelly KL (1958) Centroid notations for the revised ISCC-NBC color name blocks. J Res Nat Bur Standards USA 61:427
Kumar Y, Goodfellow M (2008) Five new species of the Streptomyces violaceusniger 16 S rRNA gene clade: Streptomyces castelarensis comb. nov., Streptomyces himastatinicus sp. nov., S. mordarskii sp. nov., S. rapamycinicus sp. nov. and S. ruanii sp. nov. Int J Syst Evol Microbiol 58:1369–1378
Kumar Y, Aiemsum-Ang P, Ward AC, Goodfellow M (2007) Diversity and geographical distribution of members of the Streptomyces violaceusniger 16 S rRNA gene clade detected by clade-specific PCR primers. FEMS Microbiol Ecol 62:54–63
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
Lane DJ (1991) 16 S/23 S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–148
Lanoot B, Vancanneyt M, Hoste B, Vandameulebroecke K, Cnockaert MC, Dawyndt P, Liu Z, Huang Y, Swings J (2005) Grouping streptomycetes using 16 S-ITS RFLP fingerprinting. Res Microbiol 156:755–762
Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 20:435–443
Liu Z, Shi Y, Zhang Y, Zhou Z, Lu Z, Li W, Huang Y, Rodriguez C, Goodfellow M (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
Loper JE (1998) Role of fluorescent siderophore production in biological control of P. ultimum by P. fluorescens strain. Phytopathology 78:166–172
Mahadevan B, Crawford DL (1997) Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzyme Microb Technol 20:489–493
Manfio GP, Zakrzewska-Czerwinska J, Atalan E, Goodfellow M (1995) Towards minimal standards for the description of Streptomyces species. Biotechnologia 7–8:242–253
Merckx R, Dijkra A, Hartog AD, Veen JAV (1987) Production of root-derived material and associated microbial growth in soil at different nutrient levels. Biol Fertil Soils 5:126–132
Paterson E, Rattray EAS, Killham K (1995) Rhizosphere ecophysiology. Encyclopedia of environmental biology, vol 3. Academic, New York, pp 237–245
Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156
Pridham TG, Hesseltine CW, Benedict RG (1958) A guide for the classification of Streptomyces according to selected groups. Appl Microbiol 6:52–79
Ramachandra M, Crawford DL, Hertel G (1988) Characterization of an extracellular lignin peroxidase of the lignocellulolytic actinomycete Streptomyces viridosporus. Appl Environ Microbiol 54:3057–3063
Saintpierre D, Amir H, Pineau R, Sembiring L, Goodfellow M (2003) Streptomyces yatensis sp. nov., a novel bioactive streptomycete isolated from a New-Caledonian ultramafic soil. Antonie van Leeuwenhoek 83:21–26
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Technical note 101. MIDI, Newark
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
Shirling EB, Gottlieb D (1966) Methods for characterisation of Streptomyces species. Int J Syst Bacteriol 16:313–340
Staneck JL, Roberts G (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231
Strap JL, Crawford DL (2006) Ecology of Streptomyces in soil and rhizosphere. In: Cooper J, Rao JR (eds) Molecular approaches to soil, rhizosphere and plant microorganism analysis. CABI Publishing, Wallingford, UK, pp 166–182
Suzuki S, Yamamoto K, Okuda T, Nishio M, Nakanishi N, Komatsubara S (2000) Selective isolation and distribution of Actinomadura rugatobispora strains in soil. Actinomycetologica 14:27–33
Thomas T, Crawford DL (1998) Cloning of clustered Streptomyces viridosporus T7A lignocellulose catabolism genes encoding peroxidase and endoglucanase and their extracellular expression in Pichia pastoris. Can J Microbiol 44:364–372
Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH et al (2002) Novel plant-microbe rhizosphere involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Trejo-Estrada SR, Paszczynski A, Crawford DL (1998a) Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED9. J Ind Microbiol Biotechnol 21:81–90
Trejo-Estrada SR, Sepulveda SR, Crawford DL (1998b) In vitro and in vivo antagonism of Streptomyces violaceusniger YCED9 against fungal pathogens of turfgrass. World J Microbiol Biotechnol 14:865–872
Tresner HD, Davies MC, Backus EJ (1961) Microscopy of Streptomyces spore morphology and its role in species differentiation. J Bacteriol 81:70–80
Tuncer M, Kuru A, Isikli M, Sahin N, Celenk FG (2004) Optimization of extracellular endoxylanase, endoglucanase and peroxidase production by Streptomyces sp. F2621 isolated in Turkey. J Appl Microbiol 97:783–791
Tuncer M, Kuru A, Sahin N, Isikli M, Isik K (2009) Production and partial characterization of extracellular peroxidase produced by Streptomyces sp. F6616 isolated in Turkey. Ann Microbiol 59(2):323–334
Upton M (1994) Ecological approaches to the selective isolation of actinomycetes for bioactivity screening. PhD Thesis, University of Newcastle, Newcastle upon Tyne, UK
Uren NC (2000) Types, amounts, and possible functions of compunds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Dekker, New York, pp 19–40
Ward AC, Goodfellow M (2004) Phylogeny and functionality: taxonomy as a roadmap to genes. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM, Washington, pp 288–313
Watson ET, Williams ST (1974) Studies on the ecology of actinomycetes in soil. VII. Actinomycetes in a coastal belt. Soil Biol Biochem 6:43–52
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
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. Williams and Wilkins, Baltimore, pp 2452–2492
Xu C, Wang L, Cui Q, Huang Y, Liu Z, Zheng G, Goodfellow M (2006) Neutrotolerant acidophilic 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
Zaehner H, Fiedler H (1995) The need for new antibiotics: possible ways forward. In: Hunter PA, Darby GK, Russell NJ (eds) Fifty years of antimicrobials: past perspective and future trends. SGM symposium 53. Cambridge University Press, Cambridge, pp 67–85
Acknowledgements
This research was supported by The Basic Sciences Research Group (TBAG) of Scientific and Technological Research Council of Turkey (TUBITAK; project no. 106T029).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sahin, N., Sazak, A., Güven, K. et al. Diversity of members of the Streptomyces violaceusniger 16S rRNA gene clade in the legumes rhizosphere in Turkey. Ann Microbiol 60, 669–684 (2010). https://doi.org/10.1007/s13213-010-0112-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-010-0112-6