Phylogenetic Study of the Species Within the Family Streptomycetaceae
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Antonie van Leeuwenhoek DOI 10.1007/s10482-011-9656-0 ORIGINAL PAPER 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 Ó Springer Science+Business Media B.V. (outside the USA) 2011 Abstract Species of the genus Streptomyces, which any other microbial genus, resulting from academic constitute the vast majority of taxa within the family and industrial activities. The methods used for char- Streptomycetaceae, are a predominant component of acterization have evolved through several phases over the microbial population in soils throughout the world the years from those based largely on morphological and have been the subject of extensive isolation and observations, to subsequent classifications based on screening efforts over the years because they are a numerical taxonomic analyses of standardized sets of major source of commercially and medically impor- phenotypic characters and, most recently, to the use of tant secondary metabolites. Taxonomic characteriza- molecular phylogenetic analyses of gene sequences. tion of Streptomyces strains has been a challenge due The present phylogenetic study examines almost all to the large number of described species, greater than described species (615 taxa) within the family Strep- tomycetaceae based on 16S rRNA gene sequences Electronic supplementary material The online version and illustrates the species diversity within this family, of this article (doi:10.1007/s10482-011-9656-0) contains which is observed to contain 130 statistically supplementary material, which is available to authorized users. D. P. Labeda (&) Z. Liu National Center for Agricultural Utilization Research, State Key Laboratory of Microbial Resources, USDA-ARS, 1815 North University Street, Peoria, Institute of Microbiology, Chinese Academy of Sciences, IL 61604, USA Beijing 100080, People’s Republic of China e-mail: [email protected] J. Chun M. Goodfellow Á R. Brown Á A. C. Ward School of Biological Sciences, Seoul National University, School of Biology, University of Newcastle, Shillim-dong, Kwanak-gu, Seoul 151-742, Newcastle upon Tyne NE1 7RU, UK Republic of Korea B. Lanoot Á M. Vanncanneyt Á J. Swings T. Tamura Á A. Oguchi Á T. Kikuchi Á H. Kikuchi Á BCCM/LMG Bacteria Collection, Department of T. Nishii Á K. Tsuji Á Y. Yamaguchi Á A. Tase Á Biochemistry, Physiology and Microbiology, Universiteit M. Takahashi Á T. Sakane Á K. I. Suzuki Á K. Hatano Gent, K. L. Ledeganckstraat 35, 9000 Ghent, Belgium NITE Biological Resource Center (NBRC), National Institute of Technology and Evaluation, S.-B. Kim 2-5-8 Kazusakamatari, Kisarazu, Department of Microbiology and Molecular Biology, Chiba 292-0818, Japan School of Bioscience and Biotechnology, Chungnam National University, 220 Gung-dong, Yusong, Daejeon 305-764, Republic of Korea 123 Antonie van Leeuwenhoek supported clades, as well as many unsupported and strains of species assigned to these genera were sent, single member clusters. Many of the observed clades are under code, to at least three experts in different consistent with earlier morphological and numerical countries. The strains were examined in each labora- taxonomic studies, but it is apparent that insufficient tory using strictly standardized media and experimen- variation is present in the 16S rRNA gene sequence tal conditions to determine morphological and within the species of this family to permit bootstrap- pigmentation properties, and carbon utilization pro- supported resolution of relationships between many of files (Shirling and Gottlieb 1966). The characters the individual clusters. evaluated had been selected based on data from previous international cooperative studies (Ku¨ster Keywords Actinobacteria Á Systematics Á 1959; Gottlieb 1961, 1963). The methods and descrip- Streptomycetales Á Actinomycetes 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 Introduction genera Streptomyces and Streptoverticillium in the eighth edition of Bergey’s Manual of Determinative The systematics of the genus Streptomyces have had a Bacteriology was based on the results of the Interna- long and convoluted history with numerous different tional Streptomyces Project (Pridham and Tresner approaches taken to the delineation of species within 1974). the genus. Early descriptions of species relied heavily The ISP study, like earlier attempts to classify on morphologically procedures, such as colour of streptomycetes, was largely based on a limited number aerial and substrate mycelia and spore chain morphol- of features, with a heavy emphasis on morphology and ogy along with rudimentary physiological features pigmentation. Sneath (1970) considered that a rigor- (Krainsky 1914; Waksman and Curtis 1916; Waksman ous application of the numerical taxonomic procedure 1919). However, substantial interest in the genus only provided the only way of reclassifying the plethora of arose because of their commercial potential following Streptomyces species since reliance on a few selected the discoveries of actinomycin and streptomycin by characters could not be expected to reveal natural Streptomyces antibioticus (Waksman and Woodruff phenetic groups. The first comprehensive numerical 1941) and Streptomyces griseus (Schatz et al. 1944), taxonomic study of the genus Streptomyces was respectively. The advent of large-scale industrial undertaken by Williams et al. (1983) who assigned isolation and screening of Streptomyces species type strains of Streptomyces species to 23 major (6–71 resulted in the naming of approximately 3,000 species strains), 20 minor (2–5 strains) and 25 single mem- by 1970, mainly on the basis of small differences in bered clusters which were named, where possible, morphological and cultural properties, with many of after the earliest validly described species they these new names found only in the patent literature contained. The minor and single membered clusters (Trejo 1970). were considered to be species and the major clusters The problems facing streptomycete systematists species-groups. The largest cluster, the Streptomyces were addressed in a series of cooperative studies, albidoflavus species-group, encompassed three sub- the most notable of which was the International groups which were recovered as separate, albeit related, Streptomyces Project (ISP). The project was planned clusters in an extension of the earlier study (Goodfellow and enacted by the Subcommittee on Taxonomy of et al. 1992). Most of the major clusters defined by Actinomycetes of the International Committee on Williams and his colleagues were recognized in an even Bacteriological Nomenclature and the Subcommittee more extensive numerical taxonomic study carried out of Actinomycetales of the Committee on Taxonomy of by Ka¨mpfer et al. (1991). The circumscription of most the American Society of Microbiology. The primary Streptomyces species described in Bergey’s Manual of aim of the study was to provide reliable descriptions of Systematic Bacteriology, volume 4 (Williams et al. extant and authentic type strains of Streptomyces and 1989) is based on the numerical taxonomic survey of Streptoverticillium species. Existing type and neotype Williams et al. (1983). 123 Antonie van Leeuwenhoek Relatively few attempts have been made to evaluate Methods phena delineated in the extensive numerical taxo- nomic surveys of streptomycetes and streptoverticillia The type strains for almost all valid species in the (Williams et al. 1983;Ka¨mpfer et al. 1991; Goodfellow family Streptomycetaceae as well as those in press on et al. 1992), using independent taxonomic approaches, October 1, 2010 were included in the study (as can be other than somewhat ad hoc studies focused on seen online in Supplemental Table 1). Some sequences representatives of specific clusters. The taxonomic were obtained from the public sequence databanks, status of some phena circumscribed by Williams and but the vast majority were determined and deposited his colleagues have been underpinned by chemotaxo- during the current study. DNA was isolated and nomic and DNA:DNA relatedness data as exemplified approximately 1320 almost-complete 16S rRNA gene by subcluster 1A (S. albidoflavus) (Mordarski et al. sequences were determined in the various collaborat- 1986; Manchester et al. 1990; Ferguson et al. 1997). In ing laboratories using previously described methods addition, Ridell et al. (1986) found that streptomycetes (Chun and Goodfellow 1995; Goodfellow et al. 2007; which shared a high number of precipitinogens Kim et al. 1996; Kumar and Goodfellow 2008; Labeda belonged to the same numerically defined clusters and Kroppenstedt 2000; Labeda et al. 2009; Lu et al. whereas those less serologically related tended to fall 2001; Park et al. 2005). into different clusters. In contrast, other taxa, such as Sequence data were organized, aligned and sub- clusters 10 (Streptomyces fulvissimus), 17 (Streptomy- jected to preliminary analysis within the ARB software ces griseoviridis), 18 (Streptomyces cyaneus) and 61 package (Ludwig et al. 2004). Duplicate sequences for (Streptomyces lavendulae)