Streptomyces leeuwenhoekii sp. nov., the producer of chaxalactins and chaxamycins, forms a distinct branch in Streptomyces gene trees

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 105, Issue 5, 2014, Pages 849-861

  Busarakam, Kanungnid ^a   Bull, Alan T ^b   Girard, Geneviève ^c   Labeda, David P ^d   Van Wezel, Gilles P ^c   Goodfellow, Michael ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

^c LEIDEN UNIVERSITY   (Netherlands)

^d NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

Author keywords

Atacama Desert; Genome sequence; Natural products; Polyphasic taxonomy; Streptomyces

Indexed keywords

ANTIBIOTIC AGENT; CHAXALACTIN DERIVATIVE; CHAXAMYCIN DERIVATIVE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL DNA; MACROLIDE; RIBOSOME DNA; RIFAMYCIN; RNA 16S;

16S RRNA GENE; ALLELE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATE; BIOSYNTHESIS; CHEMOTAXONOMY; CLASSIFICATION; CONTROLLED STUDY; GENE SEQUENCE; GENETIC ASSOCIATION; HOUSEKEEPING GENE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; PHYLOGENETIC TREE; PREDICTION; PRIORITY JOURNAL; STREPTOMYCES; STREPTOMYCES CHIANGMAIENSIS; STREPTOMYCES HYDERABADENSIS; STREPTOMYCES LEEUWENHOEKII; TAXONOMY; BACTERIUM IDENTIFICATION; CHEMISTRY; CLUSTER ANALYSIS; DESERT CLIMATE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; SCANNING ELECTRON MICROSCOPY;

STREPTOMYCES;

ANTI-BACTERIAL AGENTS; BACTERIAL TYPING TECHNIQUES; CLUSTER ANALYSIS; DESERT CLIMATE; DNA, BACTERIAL; DNA, RIBOSOMAL; MACROLIDES; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; RIFAMYCINS; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY; STREPTOMYCES;

EID: 84900811629     PISSN: 00036072     EISSN: 15729699     Source Type: Journal    
DOI: 10.1007/s10482-014-0139-y     Document Type: Article

References (67)

1. 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
2. Bentley SD, Chater KF, Cerdeno-Tarraga AM et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147 (Pubitemid 34506788)
3. Bérdy J (2012) Thought and facts about antibiotics: where are we now and where are we heading. J Antibiot (Tokyo) 51:1-26
4. Bull AT, Asenjo JA (2013) Microbiology of hyper-arid environments: recent insights from the Atacama Desert. Antonie Van Leeuwenhoek 103:1173-1179
5. Busti E, Monciardini P, Cavaletti L, Bamonte R, Lazzarini A, Sosio M, Donadio S (2006) Antibiotic-producing ability by representatives of newly discovered lineages of actinomycetes. Microbiology 152:675-683
6. Chandra G, Chater KF (2014) Developmental biology of Streptomyces from the perspective of 100 actinobacterial gene sequences. FEMS Microbiol Rev. (in press)
7. Collins MD, Goodfellow M, Minnikin DE, Alderson G (1985) Menaquinone composition of mycolic acid containing actinomycetes and some sporoactinomycetes. J Appl Bacteriol 58:77-86 (Pubitemid 15136131)
8. Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F et al (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
9. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797
11. Felsenstein J (1981) Evolutionary trees from DNA sequences: maximum likelihood approach. J Mol Evol 17:368-376
12. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
13. Fitch WM (1971) Towards defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406-416
14. Gao B, Gupta RS (2012) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76:66-111
15. 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
16. Gómez-Silva B, Rainey FA, Warren-Rhodes KA, Mc Kay CP, Navarro-González R (2008) Atacama Desert soil microbiology. In: Dion P, Nautinal CS (eds) Microbiology of extreme soils, soil biology 13. Springer, Berlin, pp 117-132
17. Goodfellow M, Fiedler HP (2010) A guide to successful bioprospecting: informed by actinobacterial systematics. Antonie Van Leeuwenhoek 98:119-142
18. Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenetics by maximum likelihood. Syst Biol 52:696-704 (Pubitemid 37365050)
19. Guo Y, Zheng W, Rong X, Huang Y (2008) A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149-159 (Pubitemid 351843556)
20. Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29:319-322 (Pubitemid 14176930)
21. Hohmann C, Schneider K, Bruntner C, Irran E, Nicholson G, Bull AT, Jones AL, Brown R, Stach JEM, Goodfellow M, Beil W, Krämer M, Imhoff JF, Süssmuth RO, Fiedler H-P (2009) Caboxamycin, a new antibiotic of the benzoxazole family produced by the deep-sea strain Streptomyces NTK 937. J Antibiot (Tokyo) 62:99-104
22. Jensen P (2010) Linking species concepts to natural product discovery in the post-genomic era. J Ind Microbiol Biotechnol 37:219-224
23. Jolley K, Maiden M (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595
24. Jones KL (1949) Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141-145
25. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, London, pp 21-132
26. Kämpfer P (2012) Genus I. Streptomyces Waksman and Henrici 1943, 339AL emend. Witt and Stackebrandt 1990, 370, emend. Wellington, Stackebrandt, Sanders, Wolstrup and Jorgensen 1992, 159. In: Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I, Ludwig W, Whitman WB (eds) Bergey's manual of systematic bacteriology, Part B, vol 5, 2nd edn. Springer, New York, pp 1455-1767
27. Kawato M, Shinobu R (1959) On Streptomyces herbaricolor sp. nov., supplement: a simple technique for microscopical observation. Mem Osaka Univ Lib Arts Educ B Nat Sci 8:114-119
28. Kim S-B, Goodfellow M (2002) Streptomyces thermospinisporus sp. nov., a moderately thermophilic carboxydotrophic streptomycete isolated from soil. Int J Syst Evol Microbiol 52:1225-1228
29. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing ExTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716-721
30. Kimura M (1980) A simple method for estimating evolutionary rates base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120
31. Klenk H-P, Goker G (2010) En route to genomic-based classification of archaea and bacteria. Syst Appl Microbiol 33:175-182
32. Labeda DP (2011) Multilocus sequence analysis of phytopathogenic Streptomyces species. Int J Syst Evol Microbiol 61:2525-2531
33. Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot C, Vanncanneyt M, Swings J, Kim S-B, 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
34. Labeda DP, Doroghazi JP, Ju K-S, Metcalf WW. (2014) Taxonomic evaluation of Streptomyces albus and related species using multilocus sequence analysis and proposals to emend the description of Streptomyces albus and describe Streptomyces pathocidini sp. nov. Int J Syst Evol Microbiol 64. (in press)
35. 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
36. Meier-Kolthoff JP, Göker M, Spöer C, Klenk H-P (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413-418
37. Murray PR, Baron EJ, Phaller MA, Ternover JC, Yolkken RJ (1999) Manual of clinical microbiology, 7th edn. ASM Press, Washington DC
38. Nachtigall J, Kulik Helaly S, Bull AT, Goodfellow M, Asenjo JA, Maier A, Wiese J, Inhoff JF, Süssmuth R-D, Fiedler H-P (2011) Atacamycins A-C, 22 membered antitumor macrolide derivatives produced by Streptomyces sp. C38. J Antibiot (Tokyo) 64:775-780
39. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
40. O'Donnell AG, Falconer C, Goodfellow M, Ward AC, Williams E (1993) Biosystematics and diversity amongst novel carboxydotrophic actinomycetes. Antonie Van Leeuwenhoek 64:325-340 (Pubitemid 24151596)
41. Okoro CK, Brown R, Jones AL, Andrews BA, Asenjo JA, Goodfellow M, Bull AT (2009) Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile. Antonie Van Leeuwenhoek 95:121-133
42. Promnuan Y, Kudo T, Ohkama M, Chantawannakul P (2013) Streptomyces chiangmaiensis sp. nov. and Streptomyces lannensis sp. nov., isolated from the South-East Asian stingless bee (Tetragonilla collina). Int J Syst Evol Microbiol 63:1896-1901
43. Rateb ME, Houssen WE, Arnold M, Abdelrahman M-H, Deng H, Harrison WTA, Okoro CK, Asenjo JA, Andrews BA, Ferguson G, Bull AT, Goodfellow M, Ebel R, Jaspars M (2011a) Chaxamycins A-D, bioactive ansamycins from a hyper-arid desert Streptomyces sp. J Nat Prod 74:1965-1971
44. Rateb ME, Houssen WE, Harrison WT, Deng H, Okoro CK, Asenjo JA, Andrews BA, Bull AT, Goodfellow M, Ebel R, Jaspars M (2011b) Diverse metabolic profiles of a Streptomyces strain isolated from a hyper-arid environment. J Nat Prod 74:1491-1499
45. Reddy TV, Mahmood S, Paris L, Reddy YH, Wellington EMH, Idris MM (2011) Streptomyces hyderabadensis sp. nov. an actinomycete isolated from soil. Int J Syst Evol Microbiol 61:76-80
46. Rong X, Huang Y (2010) Taxonomic evaluation of the Streptomyces griseus clade using mulitilocus sequence analysis and DNA-DNA hybridization, with proposal to combine 29 species and three subspecies as 11 genomic species. Int J Syst Evol Microbiol 60:696-703
47. Rong X, Huang Y (2012) Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for the systematics of the whole genus. Syst Appl Microbiol 35:7-18
48. Rong X, Guo Y, Huang Y (2009) Proposal to reclassify the Streptomyces albidoflavus clade based on the basis of multilocus sequence analysis and DNA-DNA hybridization, and taxonomic elucidation of Streptomyces griseus subsp. solvifaciens. Syst Appl Microbiol 32:314-322
49. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
50. Santhanam R, Okoro CK, Rong X, Huang Y, Bull AT, Woen Y, Andrews BA, Asenjo JA, Goodfellow M (2012a) Streptomyces atacamensis sp. nov., isolated from an extreme hyper-arid soil of the Atacama Desert. Int J Syst Evol Microbiol 62:2680-2684
51. Santhanam R, Okoro CK, Rong X, Huang Y, Bull AT, Andrews BA, Asenjo AJ, Weon HY, Goodfellow M (2012b) Streptomyces deserti sp. nov., isolated from hyper-arid desert soil. Antonie Van Leeuwenhoek 101:575-581
52. Santhanam R, Rong X, Huang Y, Andrews BA, Asenjo JA, Goodfellow M (2013) Streptomyces bullii sp nov., isolated from a hyper-arid Atacama Desert soil. Antonie Van Leeuwenhoek 103:367-373
53. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. MIDI Inc., Newark
54. Schulze D, Beese P, Ohlendorf B, Erhard A, Zinecker H, Dorador C, Imhoff J (2011) Abenquines A-D: aminoquinone derivatives produced by Streptomyces sp. strain DB634. J Antibiot Tokyo 64:763-768
55. Sentausa E, Fournier PE (2013) Advantages and limitations of genomics in prokaryotic taxonomy. Clin Microbiol Infect 19:790-795
56. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Evol Microbiol 16:313-340
57. Sutcliffe IC, Trujillo ME, Goodfellow M (2012) A call to arms for systematists: revitalizing the purpose and practices underpinning the description of novel microbial taxa. Antonie Van Leeuwenhoek 101:13-20
58. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512-526 (Pubitemid 23157236)
59. 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
60. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680 (Pubitemid 24354800)
61. 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
62. Wayne LG, Brenner DJ, Colwell RR, Grimont PAB, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) International Committee on systematic bacteriology report on the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463-464
63. Whitman WB (2011) Intent of the nomenclatural code and recommendations about naming species based on genomic sequences. The Bulletin of BIMIS 2:135-139
64. 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
65. Williams PG (2008) Panning for chemical gold: marine bacteria as a source of new therapeutics. Trends Biotechnol 27:45-52
66. Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ (1983) Numerical classification of Streptomyces and related genera. J Gen Microbiol 129:1743-1813 (Pubitemid 13044278)
67. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using Bruijn graphs. Genome Res 18:821-829 (Pubitemid 351645072)