A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics.

Streptomycetes are a complex group of actinomycetes that produce diverse bioactive metabolites of commercial significance. Systematics can provide a useful framework for identifying species that may produce novel metabolites. However, previously proposed approaches to the systematics of Streptomyces have suffered from either poor interlaboratory comparability or insufficient resolution. In particular, the Streptomyces griseus 16S rRNA gene clade is the most challenging and least defined group within the genus Streptomyces in terms of phylogeny. Here we report the results of a multilocus sequence analysis scheme developed to address the phylogeny of this clade. Sequence fragments of six housekeeping genes, atpD, gyrB, recA, rpoB, trpB and 16S rRNA, were obtained for 53 reference strains that represent 45 valid species and subspecies. Analysis of each individual locus confirmed the suitability of loci and the congruence of single-gene trees for concatenation. Concatenated trees of three, four, five and all six genes were constructed, and the stability of the topology and discriminatory power of each tree were analysed. It can be concluded from the results that phylogenetic analysis based on multilocus sequences is more accurate and robust for species delineation within Streptomyces. A multilocus phylogeny of six genes proved to be optimal for elucidating the interspecies relationships within the S. griseus 16S rRNA gene clade. Our multilocus sequence analysis scheme provides a valuable tool that can be applied to other Streptomyces clades for refining the systematic framework of this genus.

[1]  Keith A. Jolley,et al.  First Insights into the Evolution of Streptococcus uberis: a Multilocus Sequence Typing Scheme That Enables Investigation of Its Population Biology , 2006, Applied and Environmental Microbiology.

[2]  P. Dawyndt,et al.  BOX-pCR fingerprinting as a powerful tool to reveal synonymous names in the genus Streptomyces. Emended descriptions are proposed for the species Streptomyces cinereorectus, S. fradiae, S. tricolor, S. colombiensis, S. filamentosus, S. vinaceus and S. phaeopurpureus. , 2004, Systematic and applied microbiology.

[3]  P. Wiener,et al.  Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters , 2001, Antonie van Leeuwenhoek.

[4]  M. Maiden,et al.  Multilocus Sequence Typing System forCampylobacter jejuni , 2001, Journal of Clinical Microbiology.

[5]  Sudhir Kumar,et al.  MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment , 2004, Briefings Bioinform..

[6]  M. Kilian,et al.  Multilocus sequence phylogenetic study of the genus Haemophilus with description of Haemophilus pittmaniae sp. nov. , 2005, International journal of systematic and evolutionary microbiology.

[7]  E. Grund,et al.  Catabolism of benzoate and monohydroxylated benzoates by Amycolatopsis and Streptomyces spp , 1990, Applied and environmental microbiology.

[8]  J. Davies,et al.  Novel Pathway of Salicylate Degradation by Streptomyces sp. Strain WA46 , 2004, Applied and Environmental Microbiology.

[9]  B. Barrell,et al.  Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) , 2002, Nature.

[10]  M. Okuhara,et al.  FR109615, a new antifungal antibiotic from Streptomyces setonii. Taxonomy, fermentation, isolation, physico-chemical properties and biological activity. , 1990, The Journal of antibiotics.

[11]  H. Baek,et al.  Phylogenetic analysis of Streptomyces spp. isolated from potato scab lesions in Korea on the basis of 16S rRNA gene and 16S-23S rDNA internally transcribed spacer sequences. , 2004, International journal of systematic and evolutionary microbiology.

[12]  Ying Huang,et al.  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. , 2005, International journal of systematic and evolutionary microbiology.

[13]  János Bérdy,et al.  Bioactive microbial metabolites. , 2005, The Journal of antibiotics.

[14]  Martin C. J. Maiden,et al.  Bioinformatics Applications Note Sequence Type Analysis and Recombinational Tests (start) , 2022 .

[15]  M. Watve,et al.  How many antibiotics are produced by the genus Streptomyces? , 2001, Archives of Microbiology.

[16]  J. Swings,et al.  Reclassification of Streptomyces nigrifaciens as a later synonym of Streptomyces flavovirens; Streptomyces citreofluorescens, Streptomyces chrysomallus subsp. chrysomallus and Streptomyces fluorescens as later synonyms of Streptomyces anulatus; Streptomyces chibaensis as a later synonym of Streptomy , 2005, International journal of systematic and evolutionary microbiology.

[17]  B. Spratt,et al.  Multilocus sequence typing. , 1999, Trends in microbiology.

[18]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[19]  E. Wellington,et al.  The taxonomy of Streptomyces and related genera. , 2001, International journal of systematic and evolutionary microbiology.

[20]  P. Dawyndt,et al.  Grouping of streptomycetes using 16S-ITS RFLP fingerprinting. , 2005, Research in microbiology.

[21]  H. Sandermann,et al.  A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. , 1992, Nucleic acids research.

[22]  U. Gophna,et al.  Multilocus sequence typing (MLST) of Escherichia coli O78 strains. , 2003, FEMS microbiology letters.

[23]  F. Ayala Molecular systematics , 2004, Journal of Molecular Evolution.

[24]  Malcolm G. P. Page,et al.  Antimicrobials , 2005, Current Opinion in Microbiology.

[25]  M. P. Cummings PHYLIP (Phylogeny Inference Package) , 2004 .

[26]  M. Achtman,et al.  Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[28]  Adam Baldwin,et al.  Multilocus Sequence Typing Scheme That Provides Both Species and Strain Differentiation for the Burkholderia cepacia Complex , 2005, Journal of Clinical Microbiology.

[29]  Jörn Piel,et al.  Metabolites from symbiotic bacteria. , 2009, Natural product reports.

[30]  D. Crawford,et al.  Isolation of lignocellulose-decomposing actinomycetes and degradation of specifically 14C-labeled lignocelluloses by six selected Streptomyces strains. , 1979, Canadian Journal of Microbiology (print).

[31]  E. B. Shirling,et al.  Methods for characterization of Streptomyces species , 1966 .

[32]  M. Maiden,et al.  Multi-locus sequence typing: a tool for global epidemiology. , 2003, Trends in microbiology.

[33]  Yoshiyuki Sakaki,et al.  Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis , 2003, Nature Biotechnology.

[34]  J P Flandrois,et al.  A multigene approach to phylogenetic analysis using the genus Mycobacterium as a model. , 2005, International journal of systematic and evolutionary microbiology.

[35]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[36]  Y. Kook,et al.  Phylogenetic analysis of the genera Streptomyces and Kitasatospora based on partial RNA polymerase beta-subunit gene (rpoB) sequences. , 2004, International journal of systematic and evolutionary microbiology.

[37]  H. Kasai,et al.  Taxonomic re-evaluation of whorl-forming Streptomyces (formerly Streptoverticillium) species by using phenotypes, DNA-DNA hybridization and sequences of gyrB, and proposal of Streptomyces luteireticuli (ex Katoh and Arai 1957) corrig., sp. nov., nom. rev. , 2003, International journal of systematic and evolutionary microbiology.

[38]  Michael A Fischbach,et al.  New antibiotics from bacterial natural products , 2006, Nature Biotechnology.

[39]  E. Hilario,et al.  Improved resolution on the phylogenetic relationships among Pseudomonas by the combined analysis of atpD, carA, recA and 16S rDNA , 2004, Antonie van Leeuwenhoek.