Phylogenetic study of the species within the family Streptomycetaceae 2011-11-10آ  phenotypic characters

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    Phylogenetic study of the species within the family Streptomycetaceae

    D. P. Labeda • M. Goodfellow • R. Brown • A. C. Ward • B. Lanoot •

    M. Vanncanneyt • J. Swings • S.-B. Kim • Z. Liu • J. Chun • T. Tamura •

    A. Oguchi • T. Kikuchi • H. Kikuchi • T. Nishii • K. Tsuji • Y. Yamaguchi •

    A. Tase • M. Takahashi • T. Sakane • K. I. Suzuki • K. Hatano

    Received: 7 September 2011 / Accepted: 7 October 2011

    � Springer Science+Business Media B.V. (outside the USA) 2011

    Abstract Species of the genus Streptomyces, which

    constitute the vast majority of taxa within the family

    Streptomycetaceae, are a predominant component of

    the microbial population in soils throughout the world

    and have been the subject of extensive isolation and

    screening efforts over the years because they are a

    major source of commercially and medically impor-

    tant secondary metabolites. Taxonomic characteriza-

    tion of Streptomyces strains has been a challenge due

    to the large number of described species, greater than

    any other microbial genus, resulting from academic

    and industrial activities. The methods used for char-

    acterization have evolved through several phases over

    the years from those based largely on morphological

    observations, to subsequent classifications based on

    numerical taxonomic analyses of standardized sets of

    phenotypic characters and, most recently, to the use of

    molecular phylogenetic analyses of gene sequences.

    The present phylogenetic study examines almost all

    described species (615 taxa) within the family Strep-

    tomycetaceae based on 16S rRNA gene sequences

    and illustrates the species diversity within this family,

    which is observed to contain 130 statistically Electronic supplementary material The online version of this article (doi:10.1007/s10482-011-9656-0) contains supplementary material, which is available to authorized users.

    D. P. Labeda (&) National Center for Agricultural Utilization Research,

    USDA-ARS, 1815 North University Street, Peoria,

    IL 61604, USA


    M. Goodfellow � R. Brown � A. C. Ward School of Biology, University of Newcastle,

    Newcastle upon Tyne NE1 7RU, UK

    B. Lanoot � M. Vanncanneyt � J. Swings BCCM/LMG Bacteria Collection, Department of

    Biochemistry, Physiology and Microbiology, Universiteit

    Gent, K. L. Ledeganckstraat 35, 9000 Ghent, Belgium

    S.-B. Kim

    Department of Microbiology and Molecular Biology,

    School of Bioscience and Biotechnology,

    Chungnam National University, 220 Gung-dong,

    Yusong, Daejeon 305-764, Republic of Korea

    Z. Liu

    State Key Laboratory of Microbial Resources,

    Institute of Microbiology, Chinese Academy of Sciences,

    Beijing 100080, People’s Republic of China

    J. Chun

    School of Biological Sciences, Seoul National University,

    Shillim-dong, Kwanak-gu, Seoul 151-742,

    Republic of Korea

    T. Tamura � A. Oguchi � T. Kikuchi � H. Kikuchi � T. Nishii � K. Tsuji � Y. Yamaguchi � A. Tase � M. Takahashi � T. Sakane � K. I. Suzuki � K. Hatano NITE Biological Resource Center (NBRC),

    National Institute of Technology and Evaluation,

    2-5-8 Kazusakamatari, Kisarazu,

    Chiba 292-0818, Japan


    Antonie van Leeuwenhoek

    DOI 10.1007/s10482-011-9656-0

  • supported clades, as well as many unsupported and

    single member clusters. Many of the observed clades are

    consistent with earlier morphological and numerical

    taxonomic studies, but it is apparent that insufficient

    variation is present in the 16S rRNA gene sequence

    within the species of this family to permit bootstrap-

    supported resolution of relationships between many of

    the individual clusters.

    Keywords Actinobacteria � Systematics � Streptomycetales � Actinomycetes


    The systematics of the genus Streptomyces have had a

    long and convoluted history with numerous different

    approaches taken to the delineation of species within

    the genus. Early descriptions of species relied heavily

    on morphologically procedures, such as colour of

    aerial and substrate mycelia and spore chain morphol-

    ogy along with rudimentary physiological features

    (Krainsky 1914; Waksman and Curtis 1916; Waksman

    1919). However, substantial interest in the genus only

    arose because of their commercial potential following

    the discoveries of actinomycin and streptomycin by

    Streptomyces antibioticus (Waksman and Woodruff

    1941) and Streptomyces griseus (Schatz et al. 1944),

    respectively. The advent of large-scale industrial

    isolation and screening of Streptomyces species

    resulted in the naming of approximately 3,000 species

    by 1970, mainly on the basis of small differences in

    morphological and cultural properties, with many of

    these new names found only in the patent literature

    (Trejo 1970).

    The problems facing streptomycete systematists

    were addressed in a series of cooperative studies,

    the most notable of which was the International

    Streptomyces Project (ISP). The project was planned

    and enacted by the Subcommittee on Taxonomy of

    Actinomycetes of the International Committee on

    Bacteriological Nomenclature and the Subcommittee

    of Actinomycetales of the Committee on Taxonomy of

    the American Society of Microbiology. The primary

    aim of the study was to provide reliable descriptions of

    extant and authentic type strains of Streptomyces and

    Streptoverticillium species. Existing type and neotype

    strains of species assigned to these genera were sent,

    under code, to at least three experts in different

    countries. The strains were examined in each labora-

    tory using strictly standardized media and experimen-

    tal conditions to determine morphological and

    pigmentation properties, and carbon utilization pro-

    files (Shirling and Gottlieb 1966). The characters

    evaluated had been selected based on data from

    previous international cooperative studies (Küster

    1959; Gottlieb 1961, 1963). The methods and descrip-

    tions resulting from these studies were published

    (Shirling and Gottlieb 1968a, b, 1969, 1972) and the

    type strains deposited in several internationally rec-

    ognized service collections. The classification of the

    genera Streptomyces and Streptoverticillium in the

    eighth edition of Bergey’s Manual of Determinative

    Bacteriology was based on the results of the Interna-

    tional Streptomyces Project (Pridham and Tresner


    The ISP study, like earlier attempts to classify

    streptomycetes, was largely based on a limited number

    of features, with a heavy emphasis on morphology and

    pigmentation. Sneath (1970) considered that a rigor-

    ous application of the numerical taxonomic procedure

    provided the only way of reclassifying the plethora of

    Streptomyces species since reliance on a few selected

    characters could not be expected to reveal natural

    phenetic groups. The first comprehensive numerical

    taxonomic study of the genus Streptomyces was

    undertaken by Williams et al. (1983) who assigned

    type strains of Streptomyces species to 23 major (6–71

    strains), 20 minor (2–5 strains) and 25 single mem-

    bered clusters which were named, where possible,

    after the earliest validly described species they

    contained. The minor and single membered clusters

    were considered to be species and the major clusters

    species-groups. The largest cluster, the Streptomyces

    albidoflavus species-group, encompassed three sub-

    groups which were recovered as separate, albeit related,

    clusters in an extension of the earlier study (Goodfellow

    et al. 1992). Most of the major clusters defined by

    Williams and his colleagues were recognized in an even

    more extensive numerical taxonomic study carried out

    by Kämpfer et al. (1991). The circumscription of most

    Streptomyces species described in Bergey’s Manual of

    Systematic Bacteriology, volume 4 (Williams et al.

    1989) is based on the numerical taxonomic survey of

    Williams et al. (1983).

    Antonie van Leeuwenhoek


  • Relatively few attempts have been made to evaluate

    phena delineated in the extensive numerical taxo-

    nomic surveys of streptomycetes and streptoverticillia

    (Williams et al. 1983; Kämpfer et al. 1991; Goodfellow

    et al. 1992), using independent taxonomic approaches,

    other than somewhat ad hoc studies focused on

    representatives of specific clusters. The taxonomic

    status of some phena circumscribed by Williams and

    his colleagues have been underpinned by chemotaxo-

    nomic and DNA:DNA relatedness data as exemplified

    by subcluster 1A (S. albidoflavus) (Mordarski et al.

    1986; Manchester et al. 1990; Ferguson et al. 1997). In

    addition, Ridell et al. (1986) found that streptomycetes

    which shared a high number of precipitinogens

    belonged to the same numerically defined clus