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Review Article International Journal of Systematic and Evolutionary Microbiology (2001), 51, 797–814 Printed in Great Britain The taxonomy of Streptomyces and related REVIEW genera ARTICLE 1 Natural Products Drug Annaliesa S. Anderson1 and Elizabeth M. H. Wellington2 Discovery Microbiology, Merck Research Laboratories, PO Box 2000, RY80Y-300, Rahway, Author for correspondence: Annaliesa Anderson. Tel: j1 732 594 4238. Fax: j1 732 594 1300. NJ 07065, USA e-mail: liesaIanderson!merck.com 2 Department of Biological Sciences, University of The streptomycetes, producers of more than half of the 10000 documented Warwick, Coventry bioactive compounds, have offered over 50 years of interest to industry and CV4 7AL, UK academia. Despite this, their taxonomy remains somewhat confused and the definition of species is unresolved due to the variety of morphological, cultural, physiological and biochemical characteristics that are observed at both the inter- and the intraspecies level. This review addresses the current status of streptomycete taxonomy, highlighting the value of a polyphasic approach that utilizes genotypic and phenotypic traits for the delimitation of species within the genus. Keywords: streptomycete taxonomy, phylogeny, numerical taxonomy, fingerprinting, bacterial systematics Introduction trait of producing whorls were the only detectable differences between the two genera. Witt & Stacke- The genus Streptomyces was proposed by Waksman & brandt (1990) concluded from 16S and 23S rRNA Henrici (1943) and classified in the family Strepto- comparisons that the genus Streptoverticillium should mycetaceae on the basis of morphology and subse- be regarded as a synonym of Streptomyces. quently cell wall chemotype. The development of Kitasatosporia was also included in the genus Strepto- numerical taxonomic systems, which utilized pheno- myces, despite having differences in cell wall com- typic traits helped to resolve the intergeneric relation- position, on the basis of 16S rRNA similarities ships within the family Streptomycetaceae and resulted (Wellington et al., 1992). This was revoked by Zhang in the reclassification of six additional genera et al. (1997), who demonstrated that members of the (Actinopycnidium, Actinosporangium, Chainia, Ely- genus Kitasatosporia always formed a stable mono- trosporangium, Kitasatoa and Microellobosporia)to phyletic clade away from streptomycetes when the Streptomyces genus (Williams et al., 1983a; sequences from the entire 16S rRNA genes were Goodfellow et al., 1986a–d). These early numerical compared. systems utilized phenotypic characters, which were fundamentally changed by the incorporation of mol- Kineosporia and Sporichthya are both rare and share ecular biological characteristics into classification many chemotaxonomic similarities with members of systems and thus enabled considerable advances the genus Streptomyces, which led to their incor- for genus delimitation within the Actinobacteria poration into the genus (Logan, 1994). The Kineo- (Stackebrandt et al., 1997). Prior to this, the genera sporia and Sporichthya have since been reinstated as Streptomyces and Streptoverticillium were two distinct independent genera on the bases of ribosomal genera; both have cell-wall type 1 (Lechevalier & sequencing: Sporichthya is a genus of the family Lechevalier, 1970), are lysed by the same phages Sporichthyaceae of the suborder Frankineae (Stacke- (Wellington & Williams, 1981) and are phylo- brandt et al., 1997) and the Kineosporia are grouped genetically closely related (Stackebrandt & Woese, with the Kineococcus (Kudo et al., 1998). 1981). Immunodiffusion studies (Ridell et al., 1986) These changes resulted in the genus Streptomyces linked members of the genus Streptoverticillium closely being the sole member of the family Strepto- to the Streptomyces lavendulae species group. Ka$ mpfer mycetaceae. In spite of this genus unification, the et al. (1991) also found similarities using physiological current classification systems have not yet solved the tests. Gladek et al. (1985) observed differences in taxonomy within the genus, a pending issue that will be DNA–RNA pairing; this and the morphological discussed in this review. 01497 # 2001 IUMS 797 A. S. Anderson and E. M. H. Wellington Definitions range of carbon sources. More than 450 Streptomyces Definition of the genus Streptomyces species were redescribed and type strains were selected and deposited in internationally recognized culture Streptomycetes are Gram-positive aerobic members of collections. The ISP did not provide an identification the order Actinomycetales within the classis Actino- scheme, only standard methods by which one could be bacteria (Stackebrandt et al., 1997) and have a DNA achieved. Williams et al. (1983a) used a numerical GjC content of 69–78 mol% (Korn-Wendisch & taxonomic approach based on phenetic characters Kutzner, 1992). Streptomycetes produce an extensive which resulted in a reduction of the numbers of branching substrate and aerial mycelium. The sub- described Streptomyces species, the 1989 edition of strate hyphae are approximately 0n5–1n0 µm in di- Bergey’s Manual describes 142 species (Williams et al., ameter and often lack cross-walls during the vegetative 1989), in contrast to 463 species described in the 1974 phase. Growth occurs at the hyphal apices and is edition (Pridham & Tresner, 1974b). This did not accompanied by branching, thus producing a complex fully resolve the problem of overspeciation, nu- tightly woven matrix of hyphae during the vegetative merous species and subspecies were described and growth phase. As the colony ages, aerial mycelia many natural isolates did not match the reference (sporophores) are produced which develop into chains strains used to construct the identification matrices of spores (conidia) by the formation of crosswalls in (Goodfellow & Dickenson, 1985). Additional chemo- the multinucleate aerial filaments. This is followed by taxonomic and molecular methods are now used separation of individual cells directly into spores together with the numerical taxonomic methods to (Wildermuth & Hopwood, 1970). The morphological improve our understanding of species relatedness features of the aerial mycelium are regarded as more within the Streptomyces genus. These include cell wall significant for characterization than the aerial my- composition (Lechevalier & Lechevalier, 1970), phage celium and they include the mode of branching, the typing (Wellington & Williams, 1981), DNA–DNA configuration of the spore chains and the surface of the hybridization (Labeda, 1992), ELISA (Kirby & spores. The surface of the conidial wall often has Rybicki, 1986), rapid biochemical assay for utilization convoluted projections which, together with the shape of 4-methyl-umbelliferone-linked substrates (Good- and the arrangement of the spore-bearing structures, fellow et al., 1987b), comparison of ribosomal protein are characteristic of each species and were often used patterns (Ochi, 1989), low-frequency restriction frag- for the separation of Streptomyces species (Pridham et ment analysis (Beyazova & Lechevalier, 1993), and al., 1958; Korn-Wendisch & Kutzner, 1992). They can comparisons of 16S rRNA and 23S rRNA sequences be distinguished from other actinomycetes by their cell (Stackebrandt et al., 1991a, b). It is important to note wall type which is characterized as Type I sensu that many of the enumerated methods covered in this (Lechevalier & Lechevalier, 1970). The presence of - review have been applied independently, an integrated diaminopimelic acid and glycine and the absence of study to combine and evaluate a specified standard characteristic sugars are typical of this cell wall type. In group of strains is still pending. This is illustrated by addition to these traits the acyl type of the muramyl Manfio et al. (1995) who grouped together data from residues in the cell-wall peptidoglycans is acetyl 10 independent studies encompassing 293 strains from (Uchida & Seino, 1997). 22 different taxospecies and eight different chemo- taxonomic or DNA fingerprinting techniques. Not one Perspectives regarding the definition of species and taxospecies was represented by all eight tests, and to overspeciation within the genus confound matters the strains studied within the taxo- species were not consistent. The discovery of antibiotics produced by strepto- mycetes in the 1940s led to extensive screening for Numerical taxonomy of the streptomycetes novel bioactive compounds and subsequently the need for patenting led to an overclassification of the genus. Early taxonomic systems relied on phenotypic traits Producers of novel natural products were described as and streptomycetes were clustered according to new species and patented. Species described within the observed similarities and differences. Groups were genus Streptomyces increased from approximately 40 obtained using similarities in spore chain morphology, to over 3000. Many of these strains were considered to spore surface ornamentation, colour (spores, substrate be synonyms. Standard identification criteria and type mycelium and soluble pigments) and the production of strains were needed to prevent overspeciation. In 1964, melanin pigment. These groups were further sub- the International Streptomyces Project (ISP) was divided using carbon source utilization patterns initiated to introduce standard criteria for the de- (Pridham & Tresner, 1974a, b). This method has been termination of species so as to reduce the number of further developed to produce the presently accepted poorly
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