Genome mining unveils widespread natural product biosynthetic capacity in human oral microbe Streptococcus mutans

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Liu, Liwei ^a   Hao, Tingting ^a,b   Xie, Zhoujie ^a   Horsman, Geoff P ^c   Chen, Yihua ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c WILFRID LAURIER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCIN; BIOLOGICAL PRODUCT; REUTERICYCLIN; TENUAZONIC ACID;

AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BACTERIAL GENE; BIOSYNTHESIS; CHEMISTRY; DATA MINING; DRUG EFFECT; GENETICS; GENOMICS; HUMAN; METABOLISM; MICROBIOLOGY; MOUTH; MULTIGENE FAMILY; PHYLOGENY; SEQUENCE ALIGNMENT; STREPTOCOCCUS MUTANS;

AMINO ACID SEQUENCE; BACTERIOCINS; BIOLOGICAL PRODUCTS; BIOSYNTHETIC PATHWAYS; DATA MINING; GENES, BACTERIAL; GENOMICS; HUMANS; MOUTH; MULTIGENE FAMILY; PHYLOGENY; SEQUENCE ALIGNMENT; STREPTOCOCCUS MUTANS; TENUAZONIC ACID;

EID: 84995955771     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep37479     Document Type: Article

References (52)

1. Berdy, J. Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65, 385-395 (2012).
2. Molinari, G. Natural products in drug discovery: present status and perspectives. Adv Exp Med Biol 655, 13-27 (2009).
3. Staunton, J. & Weissman, K. J. Polyketide biosynthesis: a millennium review. Nat Prod Rep 18, 380-416 (2001).
4. Yu, D. Y., Xu, F. C., Zeng, J. & Zhan, J. X. Type III polyketide synthases in natural product biosynthesis. IUBMB Life 64, 285-295 (2012).
5. Strieker, M., Tanovic, A. & Marahiel, M. A. Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struc Biol 20, 234-240 (2010).
6. Du, L. C. & Lou, L. L. PKS and NRPS release mechanisms. Nat Prod Rep 27, 255-278 (2010).
7. Lambalot, R. H. et al. A new enzyme superfamily-The phosphopantetheinyl transferases. Chem Biol 3, 923-936 (1996).
8. Arnison, P. G. et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 30, 1568 (2013).
9. Cotter, P. D., Ross, R. P. & Hill, C. Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 11, 95-105 (2013).
10. Sahl, H. G. & Bierbaum, G. Lantibiotics: Biosynthesis and biological activities of uniquely modified peptides from gram-positive bacteria. Annu Rev Microbiol 52, 41-79 (1998).
11. van Belkum, M. J., Martin-Visscher, L. A. & Vederas, J. C. Structure and genetics of circular bacteriocins. Trends Microbiol 19, 411-418 (2011).
12. Hou, Y. P. et al. Structure and biosynthesis of the antibiotic bottromycin D. Org Lett 14, 5050-5053 (2012).
13. Wang, H., Fewer, D. P., Holm, L., Rouhiainen, L. & Sivonen, K. Atlas of nonribosomal peptide and polyketide biosynthetic pathways reveals common occurrence of nonmodular enzymes. P Natl Acad Sci USA 111, 9259-9264 (2014).
14. Jenke-Kodama, H., Sandmann, A., Muller, R. & Dittmann, E. Evolutionary implications of bacterial polyketide synthases. Mol Biol Evol 22, 2027-2039 (2005).
15. Guo, C. J. & Wang, C. C. C. Recent advances in genome mining of secondary metabolites in Aspergillus terreus. Front Microbiol 5, 717 (2014).
16. Calteau A. et al. Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria. BMC Genomics 15, 977 (2014).
17. Ju, K. S. et al. Discovery of phosphonic acid natural products by mining the genomes of 10,000 actinomycetes. P Natl Acad Sci USA 112, 12175-12180(2015).
18. Donia, M. S. et al. A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell 158, 1402-1414 (2014).
19. Joyner, P. M. et al. Mutanobactin A from the human oral pathogen Streptococcus mutans is a cross-kingdom regulator of the yeastmycelium transition. Org Biomol Chem 8, 5486-5489 (2010).
20. Wang, X. R., Du, L., You, J. L., King, J. B. & Cichewicz, R. H. Fungal biofilm inhibitors from a human oral microbiome-derived bacterium. Org Biomol Chem 10, 2044-2050 (2012).
21. Qi, F. X., Chen, P. & Caufield, P. W. Purification of mutacin III from group III Streptococcus mutans UA787 and genetic analyses of mutacin III biosynthesis genes. Appl Environ Microbiol 65, 3880-3887 (1999).
22. Qi, F. X., Chen, P. & Caufield, P. W. Purification and biochemical characterization of mutacin I from the group I strain of Streptococcus mutans, CH43, and genetic analysis of mutacin I biosynthesis genes. Appl Environ Microbiol 66, 3221-3229 (2000).
23. Qi, F. X., Chen, P. & Caufield, P. W. The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl Environ Microbiol 67, 15-21 (2001).
24. Novak, J. et al. Detection of modified amino acids in lantibiotic peptide mutacin II by chemical derivatization and electrospray ionization mass spectroscopic analysis. Anal Biochem 236, 358-360 (1996).
25. Kamiya, R. U., Hofling, J. F. & Goncalves, R. B. Frequency and expression of mutacin biosynthesis genes in isolates of Streptococcus mutans with different mutacin-producing phenotypes. J Med Microbiol 57, 626-635 (2008).
26. Wu, C. G. et al. Genomic island TnSmu2 of streptococcus mutans harbors a nonribosomal peptide synthetase-polyketide synthase gene cluster responsible for the biosynthesis of pigments involved in oxygen and H2O2 tolerance. Appl Environ Microbiol 76, 5815-5826 (2010).
27. Lin, X. B. et al. Genetic determinants of reutericyclin biosynthesis in Lactobacillus reuteri. Appl Environ Microbiol 81, 2032-2041 (2015).
28. Keating, T. A. et al. Chain termination steps in nonribosomal peptide synthetase assembly lines: Directed acyl-S-enzyme breakdown in antibiotic and siderophore biosynthesis. Chembiochem 2, 99-107 (2001).
29. Lohman, J. R. et al. Structural and evolutionary relationships of "AT-less" type I polyketide synthase ketosynthases. P Natl Acad Sci USA 112, 12693-12698 (2015).
30. Buchholz, T. J. et al. Polyketide beta-Branching in Bryostatin Biosynthesis: Identification of Surrogate Acetyl-ACP Donors for BryR, an HMG-ACP Synthase. Chem Biol 17, 1092-1100 (2010).
31. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: A sequence logo generator. Genome Res 14, 1188-1190 (2004).
32. Plat, A., Kluskens, L. D., Kuipers, A., Rink, R. & Moll, G. N. Requirements of the engineered leader peptide of nisin for inducing modification, export, and cleavage. Appl Environ Microbiol 77, 604-611 (2011).
33. Escano, J., Stauffer, B., Brennan, J., Bullock, M. & Smith, L. The leader peptide of mutacin 1140 has distinct structural components compared to related class I lantibiotics. Microbiologyopen 3, 961-972 (2014).
34. Robson, C. L., Wescombe, P. A., Klesse, N. A. & Tagg, J. R. Isolation and partial characterization of the Streptococcus mutans type All lantiblotic mutacin K8. Microbiology 153, 1631-1641 (2007).
35. Yonezawa, H. & Kuramitsu, H. K. Genetic analysis of a unique bacteriocin, Smb, produced by Streptococcus mutans GS5. Antimicrob Agents Chemother 49, 541-548 (2005).
36. Wang, H., Fewer, D. P. & Sivonen, K. Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS One 6, e22384 (2011).
37. Hossain, M. S. & Biswas, I. SMU.152 Acts as an Immunity Protein for Mutacin IV. J Bacteriol 194, 3486-3494 (2012).
38. Hale, J. D. F., Heng, N. C. K., Jack, R. W. & Tagg, J. R. Identification of nlmTE, the locus encoding the ABC transport system required for export of nonlantibiotic mutacins in Streptococcus mutans. J Bacteriol 187, 5036-5039 (2005).
39. Hale, J. D. F., Ting, Y. T., Jack, R. W., Tagg, J. R. & Heng, N. C. K. Bacteriocin (mutacin) production by Streptococcus mutans genome sequence reference strain UA159: elucidation of the antimicrobial repertoire by genetic dissection. Appl Environ Microbiol 71, 7613-7617 (2005).
40. Kreth, J., Merritt, J., Shi, W. & Qi, F. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J Bacteriol 187, 7193-7203 (2005).
41. Hillman, J. D. Genetically modified Streptococcus mutans for the prevention of dental caries. Antonie Van Leeuwenhoek 82, 361-366 (2002).
42. Perry, J. A., Jones, M. B., Peterson, S. N., Cvitkovitch, D. G. & Levesque, C. M. Peptide alarmone signalling triggers an auto-active bacteriocin necessary for genetic competence. Mol Microbiol 72, 905-917 (2009).
43. Dufour, D., Cordova, M., Cvitkovitch, D. G. & Levesque, C. M. Identification of a novel role associated with a streptococcal bacteriocin: regulation of the competence pathway. J Bacteriol 193, 6552-6559 (2011).
44. Donia, M. S. & Fischbach, M. A. Small molecules from the human microbiota. Science 349, 1254766 (2015).
45. Challinor, V. L. & Bode, H. B. Bioactive natural products from novel microbial sources. An Ny Acad Sci 1354, 82-97 (2015).
46. Koppel, N. & Balskus, E. P. Exploring and understanding the biochemical diversity of the human microbiota. Cell Chem Bio 23, 18-30 (2016).
47. Zipperer, A. et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature 535, 511-516 (2016).
48. Weber, T. et al. antiSMASH 3.0 - a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43, W237-W243 (2015).
49. Ziemert, N. et al. The natural product domain seeker NaPDoS. a phylogeny based bioinformatic tool to classify secondary metabolite gene diversity. PLoS One 7, e34064 (2012).
50. Rottig, M. et al. NRPSpredictor2 - a web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res 39, W362-W367 (2011).
51. Marchler-Bauer, A. et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39, D225-D229 (2011).
52. van Heel, A. J., de Jong, A., Montalban-Lopez, M., Kok, J. & Kuipers, O. P. BAGEL3: automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res 41, W448-W453 (2013).