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Analysis of novel kitasatosporae reveals significant evolutionary changes in conserved developmental genes between Kitasatospora and Streptomyces

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Abstract

Actinomycetes are antibiotic-producing filamentous bacteria that have a mycelial life style. The members of the three genera classified in the family Streptomycetaceae, namely Kitasatospora, Streptacidiphilus and Streptomyces, are difficult to distinguish using phenotypic properties. Here we present biochemical and genetic evidence that helps underpin the case for the continued recognition of the genus Kitasatospora and for the delineation of additional Kitasatospora species. Two novel Kitasatospora strains, isolates MBT63 and MBT66, and their genome sequences are presented. The cell wall of the Kitasatospora strains contain a mixture of meso-and LL-diaminopimelic acid (A2pm), whereby a single DapF surprisingly suffices to incorporate both components into the Kitasatospora cell wall. The availability of two new Kitasatospora genome sequences in addition to that of the previously sequenced Kitasatospora setae KM-6054T allows better phylogenetic comparison between kitasatosporae and streptomycetes. This showed that the developmental regulator BldB and the actin-like protein Mbl are absent from kitasatosporae, while the cell division activator SsgA and its transcriptional activator SsgR have been lost from some Kitasatospora species, strongly suggesting that Kitasatospora have evolved different ways to control specific steps in their development. We also show that the tetracycline-producing strain “Streptomyces viridifaciens” DSM 40239 not only has properties consistent with its classification in the genus Kitasatospora but also merits species status within this taxon.

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Abbreviations

aa:

Amino acid

A2pm:

Diaminopimelic acid

nt:

Nucleotide

SALP:

SsgA-like protein

References

  • Ainsa JA, Bird N, Ryding NJ, Findlay KC, Chater KF (2010) The complex whiJ locus mediates environmentally sensitive repression of development of Streptomyces coelicolor A3(2). Antonie Van Leeuwenhoek 98:225–236

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Angell S, Lewis CG, Buttner MJ, Bibb MJ (1994) Glucose repression in Streptomyces coelicolor A3(2): a likely regulatory role for glucose kinase. Mol Gen Genet 244:135–143

    Article  CAS  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1997) Currents protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75

    Article  Google Scholar 

  • Bagchi S, Tomenius H, Belova LM, Ausmees N (2008) Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol Microbiol 70:1037–1050

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8:557–563

    Article  CAS  PubMed  Google Scholar 

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  PubMed  Google Scholar 

  • Berriman M, Rutherford K (2003) Viewing and annotating sequence data with Artemis. Brief Bioinform 4:124–132

    Article  CAS  PubMed  Google Scholar 

  • Busarakam K, Bull AT, Girard G, Labeda DP, van Wezel GP, Goodfellow M (2014) Streptomyces leeuwenhoekii sp nov., the producer of chaxalactins and chaxamycins, forms a distinct branch in Streptomyces gene trees. Antonie van Leeuwenhoek 105(5):849–861

    Article  CAS  PubMed  Google Scholar 

  • Celler K, Koning RI, Koster AJ, van Wezel GP (2013) Multidimensional view of the bacterial cytoskeleton. J Bacteriol 195:1627–1636

    Article  PubMed Central  PubMed  Google Scholar 

  • Chater KF (1972) A morphological and genetic mapping study of white colony mutants of Streptomyces coelicolor. J Gen Microbiol 72:9–28

    Article  CAS  PubMed  Google Scholar 

  • Chater KF, Losick R (1997) Mycelial life style of Streptomyces coelicolor A3(2) and its relatives. In: Shapiro JA, Dworkin M (eds) Bacteria as multicellular organisms. Oxford University Press, New York, pp 149–182

    Google Scholar 

  • Claessen D, Rozen DE, Kuipers OP, Sogaard-Andersen L, van Wezel GP (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12:115–124

    Article  CAS  PubMed  Google Scholar 

  • Colson S, Stephan J, Hertrich T, Saito A, van Wezel GP, Titgemeyer F, Rigali S (2007) Conserved cis-acting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J Mol Microbiol Biotechnol 12:60–66

    Article  CAS  PubMed  Google Scholar 

  • Colson S, van Wezel GP, Craig M, Noens EE, Nothaft H, Mommaas AM, Titgemeyer F, Joris B, Rigali S (2008) The chitobiose-binding protein, DasA, acts as a link between chitin utilization and morphogenesis in Streptomyces coelicolor. Microbiology 154:373–382

    Article  CAS  PubMed  Google Scholar 

  • Craney A, Ozimok C, Pimentel-Elardo SM, Capretta A, Nodwell JR (2012) Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism. Chem Biol 19:1020–1027

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yanez-Guerra LA, Ramos-Aboites HE, Pernodet JL, Anne J, van Wezel GP, Barona-Gomez F (2013) The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol 5:1165–1175

    Article  PubMed Central  PubMed  Google Scholar 

  • Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147

    Article  PubMed Central  PubMed  Google Scholar 

  • Eccleston M, Ali RA, Seyler R, Westpheling J, Nodwell J (2002) Structural and genetic analysis of the BldB protein of Streptomyces coelicolor. J Bacteriol 184:4270–4276

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Flärdh K, Buttner MJ (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7:36–49

    Article  PubMed  Google Scholar 

  • Foulston LC, Bibb MJ (2010) Microbisporicin gene cluster reveals unusual features of lantibiotic biosynthesis in actinomycetes. Proc Natl Acad Sci U S A 107:13461–13466

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Girard G, Traag BA, Sangal V, Mascini N, Hoskisson PA, Goodfellow M, van Wezel GP (2013) A novel taxonomic marker that discriminates between morphologically complex actinomycetes. Open Biol 3:130073

    Article  PubMed Central  PubMed  Google Scholar 

  • Goodfellow M (2012) Phylum XXVI. Actinobacteria phyl. nov. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, vol 5. The Actinobacteria, parts A and B, 2nd edn. Springer, New York, pp 1–2083

  • Gourevitch A, Lein J (1955) Production of tetracycline and substituted tetracyclines. US Patent 2,712,517

  • Heichlinger A, Ammelburg M, Kleinschnitz EM, Latus A, Maldener I, Flärdh K, Wohlleben W, Muth G (2011) The MreB-like protein Mbl of Streptomyces coelicolor A3(2) depends on MreB for proper localization and contributes to spore wall synthesis. J Bacteriol 193:1533–1542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Holmes NA, Walshaw J, Leggett RM, Thibessard A, Dalton KA, Gillespie MD, Hemmings AM, Gust B, Kelemen GH (2013) Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth in Streptomyces. Proc Natl Acad Sci USA 110:E397–E406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hopwood DA (2007) Streptomyces in nature and medicine: the antibiotic makers. Oxford University Press, New York

    Google Scholar 

  • Husemann P, Stoye J (2010) r2cat: synteny plots and comparative assembly. Bioinformatics 26:570–571

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ichikawa N, Oguchi A, Ikeda H, Ishikawa J, Kitani S, Watanabe Y, Nakamura S, Katano Y, Kishi E, Sasagawa M, Ankai A, Fukui S, Hashimoto Y, Kamata S, Otoguro M, Tanikawa S, Nihira T, Horinouchi S, Ohnishi Y, Hayakawa M, Kuzuyama T, Arisawa A, Nomoto F, Miura H, Takahashi Y, Fujita N (2010) Genome sequence of Kitasatospora setae NBRC 14216T: an evolutionary snapshot of the family Streptomycetaceae. DNA Res 17:393–406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jakimowicz D, van Wezel GP (2012) Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol Microbiol 85:393–404

    Article  CAS  PubMed  Google Scholar 

  • Kämpfer P (2012) Family 1. Streptomycetaceae Waksman and Henrici 1943, 339AL emend. Rainey, Ward-Rainey and Stackebrandt, 1997, 486 emend. Kim, Lonsdale, Seong and Goodfellow 2003b, 113 emend. Zhi, Li and Stackebrandt 2009, 600. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, vol 5. 2nd edn. Springer, New York

  • Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64

    Article  CAS  PubMed  Google Scholar 

  • Kawamoto S, Watanabe H, Hesketh A, Ensign JC, Ochi K (1997) Expression analysis of the ssgA gene product, associated with sporulation and cell division in Streptomyces griseus. Microbiology 143:1077–1086

    Article  CAS  PubMed  Google Scholar 

  • Keijser BJ, Noens EE, Kraal B, Koerten HK, van Wezel GP (2003) The Streptomyces coelicolor ssgB gene is required for early stages of sporulation. FEMS Microbiol Lett 225:59–67

    Article  CAS  PubMed  Google Scholar 

  • Kirby R (2011) Chromosome diversity and similarity within the Actinomycetales. FEMS Microbiol Lett 319:1–10

    Article  CAS  PubMed  Google Scholar 

  • Kirby R, Gan TK, Hunter I, Herron P, Tilley E (2008) The genome of Streptomyces rimosus subsp. rimosus shows a novel structure compared to other Streptomyces using DNA/DNA microarray analysis. Antonie Van Leeuwenhoek 94:173–186

    Article  CAS  PubMed  Google Scholar 

  • Kirby R, Herron P, Hoskisson P (2011) Analysis of developmental gene conservation in the Actinomycetales using DNA/DNA microarray comparisons. Antonie Van Leeuwenhoek 99:159–177

    Article  PubMed  Google Scholar 

  • Kodani S, Hudson ME, Durrant MC, Buttner MJ, Nodwell JR, Willey JM (2004) The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc Natl Acad Sci USA 101:11448–11453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B, Vanncanneyt M, Swings J, Kim SB, Liu Z, Chun J, Tamura T, Oguchi A, Kikuchi T, Kikuchi H, Nishii T, Tsuji K, Yamaguchi Y, Tase A, Takahashi M, Sakane T, Suzuki KI, Hatano K (2012) Phylogenetic study of the species within the family Streptomycetaceae. Antonie Van Leeuwenhoek 101:73–104

    Article  CAS  PubMed  Google Scholar 

  • Lewis RA, Laing E, Allenby N, Bucca G, Brenner V, Harrison M, Kierzek AM, Smith CP (2010) Metabolic and evolutionary insights into the closely-related species Streptomyces coelicolor and Streptomyces lividans deduced from high-resolution comparative genomic hybridization. BMC Genom 11:682

    Article  CAS  Google Scholar 

  • Lin YS, Kieser HM, Hopwood DA, Chen CW (1993) The chromosomal DNA of Streptomyces lividans 66 is linear. Mol Microbiol 10:923–933

    Article  CAS  PubMed  Google Scholar 

  • Ludwig W, Euzeby J, Schumann P, Busse H-J, Trujillo ME, Kämpfer P, Whitman WB (2012) Road map of the phylum Actinobacteria. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, vol 5. 2nd edn. Springer, New York, pp 1–28

  • Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26:1107–1115

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McCormick JR (2009) Cell division is dispensable but not irrelevant in Streptomyces. Curr Opin Biotechnol 12:689–698

    CAS  Google Scholar 

  • Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R (2011) antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39:W339–W346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merrick MJ (1976) A morphological and genetic mapping study of bald colony mutants of Streptomyces coelicolor. J Gen Microbiol 96:299–315

    Article  CAS  PubMed  Google Scholar 

  • Noens EE, Mersinias V, Willemse J, Traag BA, Laing E, Chater KF, Smith CP, Koerten HK, van Wezel GP (2007) Loss of the controlled localization of growth stage-specific cell-wall synthesis pleiotropically affects developmental gene expression in an ssgA mutant of Streptomyces coelicolor. Mol Microbiol 64:1244–1259

    Article  CAS  PubMed  Google Scholar 

  • Omura S, Takahashi Y, Iwai Y, Tanaka H (1982) Kitasatosporia, a new genus of the order Actinomycetales. J Antibiot (Tokyo) 35:1013–1019

    Article  CAS  Google Scholar 

  • Pope MK, Green BD, Westpheling J (1996) The bld mutants of Streptomyces coelicolor are defective in the regulation of carbon utilization, morphogenesis and cell–cell signalling. Mol Microbiol 19:747–756

    Article  CAS  PubMed  Google Scholar 

  • Pope MK, Green B, Westpheling J (1998) The bldB gene encodes a small protein required for morphogenesis, antibiotic production, and catabolite control in Streptomyces coelicolor. J Bacteriol 180:1556–1562

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shendure J, Lieberman Aiden E (2012) The expanding scope of DNA sequencing. Nat Biotechnol 30:1084–1094

    Article  CAS  PubMed  Google Scholar 

  • Soliveri J, Vijgenboom E, Granozzi C, Plaskitt KA, Chater KF (1993) Functional and evolutionary implications of a survey of various actinomycetes for homologues of two Streptomyces coelicolor sporulation genes. J Gen Microbiol 139:2569–2578

    Article  CAS  PubMed  Google Scholar 

  • Soliveri JA, Gomez J, Bishai WR, Chater KF (2000) Multiple paralogous genes related to the Streptomyces coelicolor developmental regulatory gene whiB are present in Streptomyces and other actinomycetes. Microbiology 146:333–343

    CAS  PubMed  Google Scholar 

  • Soufo HJ, Graumann PL (2003) Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr Biol 13:1916–1920

    Article  PubMed  Google Scholar 

  • Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Traag BA, van Wezel GP (2008) The SsgA-like proteins in actinomycetes: small proteins up to a big task. Antonie Van Leeuwenhoek 94:85–97

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Traag BA, Kelemen GH, Van Wezel GP (2004) Transcription of the sporulation gene ssgA is activated by the IclR-type regulator SsgR in a whi-independent manner in Streptomyces coelicolor A3(2). Mol Microbiol 53:985–1000

    Article  CAS  PubMed  Google Scholar 

  • van Wezel GP, McDowall KJ (2011) The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 28:1311–1333

    Article  PubMed  Google Scholar 

  • van Wezel GP, van der Meulen J, Kawamoto S, Luiten RG, Koerten HK, Kraal B (2000) ssgA is essential for sporulation of Streptomyces coelicolor A3(2) and affects hyphal development by stimulating septum formation. J Bacteriol 182:5653–5662

    Article  PubMed Central  PubMed  Google Scholar 

  • van Wezel GP, Krabben P, Traag BA, Keijser BJ, Kerste R, Vijgenboom E, Heijnen JJ, Kraal B (2006) Unlocking Streptomyces spp. for use as sustainable industrial production platforms by morphological engineering. Appl Environ Microbiol 72:5283–5288

    Article  PubMed Central  PubMed  Google Scholar 

  • Wellington EM, Stackebrandt E, Sanders D, Wolstrup J, Jorgensen NO (1992) Taxonomic status of Kitasatosporia, and proposed unification with Streptomyces on the basis of phenotypic and 16S rRNA analysis and emendation of Streptomyces Waksman and Henrici 1943, 339AL. Int J Syst Bacteriol 42:156–160

    Article  CAS  PubMed  Google Scholar 

  • Willemse J, Borst JW, de Waal E, Bisseling T, van Wezel GP (2011) Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev 25:89–99

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Willey JM, van der Donk WA (2007) Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61:477–501

    Article  CAS  PubMed  Google Scholar 

  • Willey J, Santamaria R, Guijarro J, Geistlich M, Losick R (1991) Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65:641–650

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Traag BA, Willemse J, McMullan D, Miller MD, Elsliger MA, Abdubek P, Astakhova T, Axelrod HL, Bakolitsa C, Carlton D, Chen C, Chiu HJ, Chruszcz M, Clayton T, Das D, Deller MC, Duan L, Ellrott K, Ernst D, Farr CL, Feuerhelm J, Grant JC, Grzechnik A, Grzechnik SK, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Krishna SS, Kumar A, Marciano D, Minor W, Mommaas AM, Morse AT, Nigoghossian E, Nopakun A, Okach L, Oommachen S, Paulsen J, Puckett C, Reyes R, Rife CL, Sefcovic N, Tien HJ, Trame CB, van den Bedem H, Wang S, Weekes D, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson I, van Wezel GP (2009) Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes. J Biol Chem 284:25268–25279

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang CC, Huang CH, Li CY, Tsay YG, Lee SC, Chen CW (2002) The terminal proteins of linear Streptomyces chromosomes and plasmids: a novel class of replication priming proteins. Mol Microbiol 43:297–305

    Article  PubMed  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Z, Wang Y, Ruan J (1997) A proposal to revive the genus Kitasatospora (Omura, Takahashi, Iwai, and Tanaka 1982). Int J Syst Bacteriol 47:1048–1054

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Sandiford SK, van Wezel GP (2014a) Triggers and cues that activate antibiotic production by actinomycetes. J Ind Microbiol Biotechnol 41:371–386

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Swierstra J, Wu C, Girard G, Choi YH, van Wamel W, Sandiford S, van Wezel GP (2014b) Eliciting antibiotics active against the ESKAPE pathogens in a collection of actinomycetes isolated from mountain soils. Microbiology In the press

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Acknowledgments

We are grateful to Eric Miller and Daniel Melton for technical assistance, KB was supported by a scholarship from the Thai Royal, Government, GG by grant 10479 from the Dutch Technology Foundation (STW) to GPvW, and MG by an Emeritus Fellowship from the Leverhulme Trust.

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Authors and Affiliations

  1. Molecular Biotechnology, Institute of Biology, Leiden University, PO Box 9505, 2300 RA, Leiden, The Netherlands

    Geneviève Girard, Joost Willemse, Hua Zhu, Dennis Claessen & Gilles P. van Wezel

  2. School of Biology, Ridley Building, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK

    Kanungnid Bukarasam & Michael Goodfellow

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  1. Geneviève Girard
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  2. Joost Willemse
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  3. Hua Zhu
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Correspondence to Gilles P. van Wezel.

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Girard, G., Willemse, J., Zhu, H. et al. Analysis of novel kitasatosporae reveals significant evolutionary changes in conserved developmental genes between Kitasatospora and Streptomyces . Antonie van Leeuwenhoek 106, 365–380 (2014). https://doi.org/10.1007/s10482-014-0209-1

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