Complete genome sequence and comparative genomic analyses of the vancomycin-producing Amycolatopsis orientalis
详细信息    查看全文
  • 作者:Li Xu (1) (2)
    He Huang (3)
    Wei Wei (2)
    Yi Zhong (10) (3)
    Biao Tang (4)
    Hua Yuan (3)
    Li Zhu (2)
    Weiyi Huang (1)
    Mei Ge (2)
    Shen Yang (3)
    Huajun Zheng (5)
    Weihong Jiang (3)
    Daijie Chen (2) (6)
    Guo-Ping Zhao (3) (4) (5) (7)
    Wei Zhao (3) (4) (8) (9)

    1. Nanjing Agricultural University
    ; Nanjing ; 210095 ; China
    2. Shanghai Laiyi Center for Biopharmaceutical R&D
    ; Shanghai ; 200240 ; China
    3. CAS Key Laboratory of Synthetic Biology
    ; Institute of Plant Physiology and Ecology ; Shanghai Institutes for Biological Sciences ; Chinese Academy of Sciences ; Shanghai ; 200031 ; China
    10. Computational Biology Center
    ; Memorial Sloan Kettering Cancer Center ; New York ; NY ; 10065 ; USA
    4. State Key Laboratory of Genetic Engineering
    ; Department of Microbiology ; School of Life Sciences and Institute of Biomedical Sciences ; Fudan University ; Shanghai ; 200433 ; China
    5. Shanghai-MOST Key Laboratory of Disease and Health Genomics
    ; Chinese National Human Genome Center at Shanghai ; Shanghai ; 201203 ; China
    6. Shanghai Institute of Pharmaceutical Industry
    ; Shanghai ; 200040 ; China
    7. Department of Microbiology and Li Ka Shing Institute of Health Sciences
    ; The Chinese University of Hong Kong ; Prince of Wales Hospital ; Shatin ; New Territories ; Hong Kong ; SAR ; China
    8. China HKY Gene Technology Company Ltd
    ; Shenzhen ; Guangdong ; 518057 ; China
    9. Medical College
    ; Shenzhen University ; Shenzhen ; Guangdong ; 518060 ; China
  • 关键词:Amycolatopsis orientalis ; Complete genome sequencing ; Molecular taxonomic characteristics ; Vancomycin biosynthesis
  • 刊名:BMC Genomics
  • 出版年:2014
  • 出版时间:December 2014
  • 年:2014
  • 卷:15
  • 期:1
  • 全文大小:1,800 KB
  • 参考文献:1. Foldes, M, Munro, R, Sorrell, TC, Shanker, S, Toohey, M (1983) In-vitro effects of vancomycin, rifampicin, and fusidic acid, alone and in combination, against methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 11: pp. 21-26 CrossRef
    2. Walsh, CT, Fisher, SL, Park, IS, Prahalad, M, Wu, Z (1996) Bacterial resistance to vancomycin: five genes and one missing hydrogen bond tell the story. Chem Biol 3: pp. 21-28 CrossRef
    3. Chang, S, Sievert, DM, Hageman, JC, Boulton, ML, Tenover, FC, Downes, FP, Shah, S, Rudrik, JT, Pupp, GR, Brown, WJ, Cardo, D, Fridkin, SK (2003) Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 348: pp. 1342-1347 CrossRef
    4. Chambers, HF, Deleo, FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7: pp. 629-641 CrossRef
    5. Calfee, DP (2012) Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci, and other Gram-positives in healthcare. Curr Opin Infect Dis 25: pp. 385-394 CrossRef
    6. Guskey, MT, Tsuji, BT (2010) A comparative review of the lipoglycopeptides: oritavancin, dalbavancin, and telavancin. Pharmacotherapy 30: pp. 80-94 CrossRef
    7. Van Wageningen, AM, Kirkpatrick, PN, Williams, DH, Harris, BR, Kershaw, JK, Lennard, NJ, Jones, M, Jones, SJ, Solenberg, PJ (1998) Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem Biol 5: pp. 155-162 CrossRef
    8. Pelzer, S, Sussmuth, R, Heckmann, D, Recktenwald, J, Huber, P, Jung, G, Wohlleben, W (1999) Identification and analysis of the balhimycin biosynthetic gene cluster and its use for manipulating glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908. Antimicrob Agents Chemother 43: pp. 1565-1573
    9. Puk, O, Huber, P, Bischoff, D, Recktenwald, J, Jung, G, Sussmuth, RD, van Pee, KH, Wohlleben, W, Pelzer, S (2002) Glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908: function of a halogenase and a haloperoxidase/perhydrolase. Chem Biol 9: pp. 225-235 CrossRef
    10. Losey, HC, Peczuh, MW, Chen, Z, Eggert, US, Dong, SD, Pelczer, I, Kahne, D, Walsh, CT (2001) Tandem action of glycosyltransferases in the maturation of vancomycin and teicoplanin aglycones: novel glycopeptides. Biochemistry 40: pp. 4745-4755 CrossRef
    11. Mulichak, AM, Losey, HC, Walsh, CT, Garavito, RM (2001) Structure of the UDP-glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosynthesis of vancomycin group antibiotics. Structure 9: pp. 547-557 CrossRef
    12. Mulichak, AM, Losey, HC, Lu, W, Wawrzak, Z, Walsh, CT, Garavito, RM (2003) Structure of the TDP-epi-vancosaminyltransferase GtfA from the chloroeremomycin biosynthetic pathway. Proc Natl Acad Sci U S A 100: pp. 9238-9243 CrossRef
    13. Lu, W, Oberthur, M, Leimkuhler, C, Tao, J, Kahne, D, Walsh, CT (2004) Characterization of a regiospecific epivancosaminyl transferase GtfA and enzymatic reconstitution of the antibiotic chloroeremomycin. Proc Natl Acad Sci U S A 101: pp. 4390-4395 CrossRef
    14. Shi, R, Lamb, SS, Zakeri, B, Proteau, A, Cui, Q, Sulea, T, Matte, A, Wright, GD, Cygler, M (2009) Structure and function of the glycopeptide N-methyltransferase MtfA, a tool for the biosynthesis of modified glycopeptide antibiotics. Chem Biol 16: pp. 401-410 CrossRef
    15. Losey, HC, Jiang, J, Biggins, JB, Oberthur, M, Ye, XY, Dong, SD, Kahne, D, Thorson, JS, Walsh, CT (2002) Incorporation of glucose analogs by GtfE and GtfD from the vancomycin biosynthetic pathway to generate variant glycopeptides. Chem Biol 9: pp. 1305-1314 CrossRef
    16. Solenberg, PJ, Matsushima, P, Stack, DR, Wilkie, SC, Thompson, RC, Baltz, RH (1997) Production of hybrid glycopeptide antibiotics in vitro and in Streptomyces toyocaensis. Chem Biol 4: pp. 195-202 CrossRef
    17. Hubbard, BK, Walsh, CT (2003) Vancomycin assembly: nature's way. Angew Chem Int Ed Engl 42: pp. 730-765 CrossRef
    18. Basch, J, Chiang, SJ (2007) Cloning and expression of a cytochrome P450 hydroxylase gene from Amycolatopsis orientalis: hydroxylation of epothilone B for the production of epothilone F. J Ind Microbiol Biotechnol 34: pp. 171-176 CrossRef
    19. Zerbe, K, Pylypenko, O, Vitali, F, Zhang, W, Rouset, S, Heck, M, Vrijbloed, JW, Bischoff, D, Bister, B, Sussmuth, RD, Pelzer, S, Wohlleben, W, Robinson, JA, Schlichting, I (2002) Crystal structure of OxyB, a cytochrome P450 implicated in an oxidative phenol coupling reaction during vancomycin biosynthesis. J Biol Chem 277: pp. 47476-47485 CrossRef
    20. Marshall, CG, Broadhead, G, Leskiw, BK, Wright, GD (1997) D-Ala-D-Ala ligases from glycopeptide antibiotic-producing organisms are highly homologous to the enterococcal vancomycin-resistance ligases VanA and VanB. Proc Natl Acad Sci U S A 94: pp. 6480-6483 CrossRef
    21. Marshall, CG, Lessard, IA, Park, I, Wright, GD (1998) Glycopeptide antibiotic resistance genes in glycopeptide-producing organisms. Antimicrob Agents Chemother 42: pp. 2215-2220
    22. Jeong, H, Sim, YM, Kim, HJ, Lee, YJ, Lee, DW, Lim, SK, Lee, SJ (2013) Genome sequences of Amycolatopsis orientalis subsp. orientalis strains DSM 43388 and DSM 46075. Genome Announcements 1: pp. 4
    23. Jeong, H, Sim, YM, Kim, HJ, Lee, DW, Lim, SK, Lee, SJ (2013) Genome sequence of the vancomycin-producing Amycolatopsis orientalis subsp. orientalis strain KCTC 9412T. Genome Announcements 1: pp. 3
    24. Zhao, W, Zhong, Y, Yuan, H, Wang, J, Zheng, H, Wang, Y, Cen, X, Xu, F, Bai, J, Han, X, Lu, G, Zhu, Y, Shao, Z, Yan, H, Li, C, Peng, N, Zhang, Z, Zhang, Y, Lin, W, Fan, Y, Qin, Z, Hu, Y, Zhu, B, Wang, S, Ding, X, Zhao, GP (2010) Complete genome sequence of the rifamycin SV-producing Amycolatopsis mediterranei U32 revealed its genetic characteristics in phylogeny and metabolism. Cell Res 20: pp. 1096-1108 CrossRef
    25. Tang, B, Zhao, W, Zheng, H, Zhuo, Y, Zhang, L, Zhao, GP (2012) Complete genome sequence of Amycolatopsis mediterranei S699 based on de novo assembly via a combinatorial sequencing strategy. J Bacteriol 194: pp. 5699-5700 CrossRef
    26. Verma, M, Kaur, J, Kumar, M, Kumari, K, Saxena, A, Anand, S, Nigam, A, Ravi, V, Raghuvanshi, S, Khurana, P, Tyagi, AK, Khurana, JP, Lal, R (2011) Whole genome sequence of the rifamycin B-producing strain Amycolatopsis mediterranei S699. J Bacteriol 193: pp. 5562-5563 CrossRef
    27. Ohnishi, Y, Ishikawa, J, Hara, H, Suzuki, H, Ikenoya, M, Ikeda, H, Yamashita, A, Hattori, M, Horinouchi, S (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190: pp. 4050-4060 CrossRef
    28. Davis, JR, Goodwin, LA, Woyke, T, Teshima, H, Bruce, D, Detter, C, Tapia, R, Han, S, Han, J, Pitluck, S, Nolan, M, Mikhailova, N, Land, ML, Sello, JK (2012) Genome sequence of Amycolatopsis sp. strain ATCC 39116, a plant biomass-degrading actinomycete. J Bacteriol 194: pp. 2396-2397 CrossRef
    29. Aziz, RK, Bartels, D, Best, AA, DeJongh, M, Disz, T, Edwards, RA, Formsma, K, Gerdes, S, Glass, EM, Kubal, M, Meyer, F, Olsen, GJ, 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 Genomics 9: pp. 75 CrossRef
    30. 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, K, Oliver, S, O鈥橬eil, S, Rabbinowitsch, E, Rajandream, MA, Rutherford, K (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: pp. 141-147 CrossRef
    31. Oliynyk, M, Samborskyy, M, Lester, JB, Mironenko, T, Scott, N, Dickens, S, Haydock, SF, Leadlay, PF (2007) Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL23338. Nat Biotechnol 25: pp. 447-453 CrossRef
    32. Pittenger, RC, Brigham, RB (1956) Streptomyces orientalis n. sp., the source of vancomycin. Antibiot 6: pp. 642-647
    33. Thiemann, JE, Zucco, G, Pelizza, G (1969) A proposal for the transfer of Streptomyces mediterranei Margalith and Beretta 1960 to the genus Nocardia as Nocardia mediterranea (Margalith and Beretta) comb. nov. Arch Mikrobiol 67: pp. 147-155 CrossRef
    34. Lechevalier, MP, Prauser, H, Labeda, DP, Ruan, JS (1986) Two new genera of nocardioform actinomycetes: amycolata gen.nov. and Amycolatopsis gen. nov. Int J Syst Bacteriol 36: pp. 29-37 CrossRef
    35. Mary, P, Lechevalier, CDB, Hubert, L (1977) Chemotaxonomy of aerobic Actinomycetes: phospholipid composition. Biochem Syst Ecol 5: pp. 249-260 CrossRef
    36. Ishinaga, M, Kito, M (1974) Participation of soluble phosphatidylserine synthetase in phosphatidylethanolamine biosynthesis in Escherichia coli membrane. Eur J Biochem/FEBS 42: pp. 483-487 CrossRef
    37. Kanfer, J, Kennedy, EP (1964) Metabolism and function of bacterial lipids. II. Biosynthesis of phospholipids in Escherichia Coli. J Biol Chem 239: pp. 1720-1726
    38. Nowicka, B, Kruk, J (2010) Occurrence, biosynthesis and function of isoprenoid quinones. Biochim Biophys Acta 1797: pp. 1587-1605 CrossRef
    39. Olsen, I (1994) Chemotaxonomy of Bacteroides: a review. Acta Odontol Scand 52: pp. 354-367 CrossRef
    40. Blinov, NO, Iakubov, GZ, Sokolova, NL, Khokhlov, AS (1967) Classification of antibiotics-quinones of actinomycetic origin. Izvestiia Akademii nauk SSSR Seriia biologicheskaia 3: pp. 357-373
    41. Wang, K, Ohnuma, S (1999) Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. Trends Biochem Sci 24: pp. 445-451 CrossRef
    42. Zhi, XY, Zhao, W, Li, WJ, Zhao, GP (2012) Prokaryotic systematics in the genomics era. Antonie Van Leeuwenhoek 101: pp. 21-34 CrossRef
    43. Udwary, DW, Zeigler, L, Asolkar, RN, Singan, V, Lapidus, A, Fenical, W, Jensen, PR, Moore, BS (2007) Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc Natl Acad Sci U S A 104: pp. 10376-10381 CrossRef
    44. Banskota, AH, McAlpine, JB, Sorensen, D, Ibrahim, A, Aouidate, M, Piraee, M, Alarco, AM, Farnet, CM, Zazopoulos, E (2006) Genomic analyses lead to novel secondary metabolites. Part 3. ECO-0501, a novel antibacterial of a new class. J Antibiot (Tokyo) 59: pp. 533-542 CrossRef
    45. Anand, S, Prasad, MV, Yadav, G, Kumar, N, Shehara, J, Ansari, MZ, Mohanty, D (2010) SBSPKS: structure based sequence analysis of polyketide synthases. Nucleic Acids Res 38: pp. W487-W496 CrossRef
    46. Ansari, MZ, Yadav, G, Gokhale, RS, Mohanty, D (2004) NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res 32: pp. W405-W413 CrossRef
    47. Trauger, JW, Walsh, CT (2000) Heterologous expression in Escherichia coli of the first module of the nonribosomal peptide synthetase for chloroeremomycin, a vancomycin-type glycopeptide antibiotic. Proc Natl Acad Sci U S A 97: pp. 3112-3117 CrossRef
    48. Rausch, C, Hoof, I, Weber, T, Wohlleben, W, Huson, DH (2007) Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol Biol 7: pp. 78 CrossRef
    49. Balibar, CJ, Vaillancourt, FH, Walsh, CT (2005) Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains. Chem Biol 12: pp. 1189-1200 CrossRef
    50. Cava, F, Lam, H, de Pedro, MA, Waldor, MK (2011) Emerging knowledge of regulatory roles of D-amino acids in bacteria. Cell Mol Life Sci CMLS 68: pp. 817-831 CrossRef
    51. Woithe, K, Geib, N, Zerbe, K, Li, DB, Heck, M, Fournier Rousset, S, Meyer, O, Vitali, F, Matoba, N, Abou Hadeed, K, Robinson, JA (2007) Oxidative phenol coupling reactions catalyzed by OxyB: a cytochrome P450 from the vancomycin producing organism. implications for vancomycin biosynthesis. J Am Chem Soc 129: pp. 6887-6895 CrossRef
    52. Puk, O, Bischoff, D, Kittel, C, Pelzer, S, Weist, S, Stegmann, E, Sussmuth, RD, Wohlleben, W (2004) Biosynthesis of chloro-beta-hydroxytyrosine, a nonproteinogenic amino acid of the peptidic backbone of glycopeptide antibiotics. J Bacteriol 186: pp. 6093-6100 CrossRef
    53. Nagarajan, R (1993) Structure-activity relationships of vancomycin-type glycopeptide antibiotics. J Antibiot (Tokyo) 46: pp. 1181-1195 CrossRef
    54. Tang, B, Wang, Q, Yang, M, Xie, F, Zhu, Y, Zhuo, Y, Wang, S, Gao, H, Ding, X, Zhang, L, Zhao, G, Zheng, H (2013) ContigScape: a Cytoscape plugin facilitating microbial genome gap closing. BMC Genomics 14: pp. 289 CrossRef
  • 刊物主题:Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
  • 出版者:BioMed Central
  • ISSN:1471-2164
文摘
Background Amycolatopsis orientalis is the type species of the genus and its industrial strain HCCB10007, derived from ATCC 43491, has been used for large-scale production of the vital antibiotic vancomycin. However, to date, neither the complete genomic sequence of this species nor a systemic characterization of the vancomycin biosynthesis cluster (vcm) has been reported. With only the whole genome sequence of Amycolatopsis mediterranei available, additional complete genomes of other species may facilitate intra-generic comparative analysis of the genus. Results The complete genome of A. orientalis HCCB10007 comprises an 8,948,591-bp circular chromosome and a 33,499-bp dissociated plasmid. In total, 8,121 protein-coding sequences were predicted, and the species-specific genomic features of A. orientalis were analyzed in comparison with that of A. mediterranei. The common characteristics of Amycolatopsis genomes were revealed via intra- and inter-generic comparative genomic analyses within the domain of actinomycetes, and led directly to the development of sequence-based Amycolatopsis molecular chemotaxonomic characteristics (MCCs). The chromosomal core/quasi-core and non-core configurations of the A. orientalis and the A. mediterranei genome were analyzed reciprocally, with respect to further understanding both the discriminable criteria and the evolutionary implementation. In addition, 26 gene clusters related to secondary metabolism, including the 64-kb vcm cluster, were identified in the genome. Employing a customized PCR-targeting-based mutagenesis system along with the biochemical identification of vancomycin variants produced by the mutants, we were able to experimentally characterize a halogenase, a methyltransferase and two glycosyltransferases encoded in the vcm cluster. The broad substrate spectra characteristics of these modification enzymes were inferred. Conclusions This study not only extended the genetic knowledge of the genus Amycolatopsis and the biochemical knowledge of vcm-related post-assembly tailoring enzymes, but also developed methodology useful for in vivo studies in A. orientalis, which has been widely considered as a barrier in this field.
NGLC 2004-2010.National Geological Library of China All Rights Reserved.
Add:29 Xueyuan Rd,Haidian District,Beijing,PRC. Mail Add: 8324 mailbox 100083
For exchange or info please contact us via email.