Expanding primary metabolism helps generate the metabolic robustness to facilitate antibiotic biosynthesis in Streptomyces

mBio

Volumn 9, Issue 1, 2018, Pages

  Schniete, Jana K ^a   Cruz Morales, Pablo ^b   Selem Mojica, Nelly ^b   Fernández Martínez, Lorena T ^c   Hunter, Iain S ^a   Barona Gómez, Francisco ^b   Hoskisson, Paul A ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b Evolution of Metabolic Diversity Laboratory   (Mexico)

^c EDGE HILL UNIVERSITY   (United Kingdom)

Author keywords

Actinobacteria; Antibiotics; Evolution; Primary metabolism; Pyruvate kinase; Streptomyces

Indexed keywords

PYRUVATE KINASE; ANTIINFECTIVE AGENT;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON SOURCE; CITRIC ACID CYCLE; CONTROLLED STUDY; ENZYME KINETICS; GENE DUPLICATION; GENE EXPRESSION; GLUCONEOGENESIS; GLYCOLYSIS; HRDB GENE; NONHUMAN; PFKA2 GENE; PFKA3 GENE; PHYLOGENY; PRIORITY JOURNAL; PYK1 GENE; PYK2 GENE; PYKA GENE; PYKF GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOMYCES COELICOLOR; BIOSYNTHESIS; GENETICS; KINETICS; METABOLISM; MULTIGENE FAMILY;

ANTI-BACTERIAL AGENTS; GENE DUPLICATION; GENE EXPRESSION; KINETICS; METABOLIC NETWORKS AND PATHWAYS; MULTIGENE FAMILY; PYRUVATE KINASE; STREPTOMYCES COELICOLOR;

EID: 85043517693     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02283-17     Document Type: Article

References (44)

1. Bentley SD, Chater KF, Cerdeño-Tárraga 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. https://doi.org/10.1038/417141a.
2. Hiltner JK, Hunter IS, Hoskisson PA. 2015. Tailoring specialized metabolite production in Streptomyces. Adv Appl Microbiol 91:237–255. https://doi.org/10.1016/bs.aambs.2015.02.002.
3. Wagner A. 2008. Robustness and evolvability: a paradox resolved. Proc Biol Sci 275:91–100. https://doi.org/10.1098/rspb.2007.1137.
4. Wagner A. 2008. Gene duplications, robustness and evolutionary innovations. Bioessays 30:367–373. https://doi.org/10.1002/bies.20728.
5. Treangen TJ, Rocha EPC. 2011. Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7:e1001284. https://doi.org/10.1371/journal.pgen.1001284.
6. McLoughlin SY, Copley SD. 2008. A compromise required by gene sharing enables survival: implications for evolution of new enzyme activities. Proc Natl Acad Sci U S A 105:13497–13502. https://doi.org/10.1073/pnas.0804804105.
7. Clark LC, Hoskisson PA. 2011. Duplication and evolution of devA-like genes in Streptomyces has resulted in distinct developmental roles. PLoS One 6:e25049. https://doi.org/10.1371/journal.pone.0025049.
8. Clark LC, Seipke RF, Prieto P, Willemse J, van Wezel GP, Hutchings MI, Hoskisson PA. 2013. Mammalian cell entry genes in Streptomyces may provide clues to the evolution of bacterial virulence. Sci Rep 3:1109. https://doi.org/10.1038/srep01109.
9. Challis GL, Hopwood DA. 2003. Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100(Suppl 2): 14555–14561. https://doi.org/10.1073/pnas.1934677100.
10. Chater KF, Biró S, Lee KJ, Palmer T, Schrempf H. 2010. The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34:171–198. https://doi.org/10.1111/j.1574-6976.2009.00206.x.
11. Kim J, Copley SD. 2007. Why metabolic enzymes are essential or nonessential for growth of Escherichia coli K12 on glucose. Biochemistry 46:12501–12511. https://doi.org/10.1021/bi7014629.
12. Teichmann SA, Babu MM. 2004. Gene regulatory network growth by duplication. Nat Genet 36:492– 496. https://doi.org/10.1038/ng1340.
13. 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. https://doi.org/10.1098/rsob.130073.
14. Chater KF, Chandra G. 2006. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol Rev 30: 651– 672. https://doi.org/10.1111/j.1574-6976.2006.00033.x.
15. Tokovenko B, Rebets Y, Luzhetskyy A. 2016. Automating assessment of the undiscovered biosynthetic potential of Actinobacteria. bioRxiv https://doi.org/10.1101/036087.
16. Bibb MJ. 2005. Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 8:208–215. https://doi.org/10.1016/j.mib.2005.02.016.
17. Lenski RE, Barrick JE, Ofria C. 2006. Balancing robustness and evolvability. PLoS Biol 4:e428. https://doi.org/10.1371/journal.pbio.0040428.
18. Nowak MA, Boerlijst MC, Cooke J, Smith JM. 1997. Evolution of genetic redundancy. Nature 388:167–171. https://doi.org/10.1038/40618.
19. 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 Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75.
20. Barona-Gómez F, Cruz-Morales P, Noda-García L. 2012. What can genome-scale metabolic network reconstructions do for prokaryotic systematics? Antonie Van Leeuwenhoek 101:35– 43. https://doi.org/10.1007/s10482-011-9655-1.
21. Cruz-Morales P, Kopp JF, Martínez-Guerrero C, Yáñez-Guerra LA, Selem-Mojica N, Ramos-Aboites H, Feldmann J, Barona-Gómez F. 2016. Phylogenomic analysis of natural products biosynthetic gene clusters allows discovery of arseno-organic metabolites in model streptomycetes. Genome Biol Evol 8:1906–1916. https://doi.org/10.1093/gbe/evw125.
22. Borodina I, Siebring J, Zhang J, Smith CP, van Keulen G, Dijkhuizen L, Nielsen J. 2008. Antibiotic overproduction in Streptomyces coelicolor A3(2) mediated by phosphofructokinase deletion. J Biol Chem 283: 25186–25199. https://doi.org/10.1074/jbc.M803105200.
23. Case RJ, Boucher Y, Dahllöf I, Holmström C, Doolittle WF, Kjelleberg S. 2007. Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microbiol 73:278–288. https://doi.org/10.1128/AEM.01177-06.
24. Kämpfer P, Glaeser SP. 2012. Prokaryotic taxonomy in the sequencing era—the polyphasic approach revisited. Environ Microbiol 14:291–317. https://doi.org/10.1111/j.1462-2920.2011.02615.x.
25. Muñoz ME, Ponce E. 2003. Pyruvate kinase: current status of regulatory and functional properties. Comp Biochem Physiol B Biochem Mol Biol 135:197–218. https://doi.org/10.1016/S1096-4959(03)00081-2.
26. Gomez-Escribano JP, Song L, Fox DJ, Yeo V, Bibb MJ, Challis GL. 2012. Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chem Sci 3:2716. https://doi.org/10.1039/c2sc20410j.
27. Hodgson DA. 2000. Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42:47–238. https://doi.org/10.1016/S0065-2911(00)42003-5.
28. Obanye AIC, Hobbs G, Gardner DCJ, Oliver SG. 1996. Correlation between carbon flux through the pentose phosphate pathway and production of the antibiotic methylenomycin in Streptomyces coelicolor A3(2). Microbiology 142:133–137. https://doi.org/10.1099/13500872-142 -1-133.
29. Sauer U, Eikmanns BJ. 2005. The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. FEMS Microbiol Rev 29:765–794. https://doi.org/10.1016/j.femsre.2004.11.002.
30. Emmerling M, Dauner M, Ponti A, Fiaux J, Hochuli M, Szyperski T, Wüthrich K, Bailey JE, Sauer U. 2002. Metabolic flux responses to pyruvate kinase knockout in Escherichia coli. J Bacteriol 184:152–164. https://doi.org/10.1128/JB.184.1.152-164.2002.
31. Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, Botstein D, Rabinowitz JD. 2006. Conservation of the metabolomic response to starvation across two divergent microbes. Proc Natl Acad Sci U S A 103:19302–19307. https://doi.org/10.1073/pnas.0609508103.
32. Li X, Wang J, Li S, Ji J, Wang W, Yang K. 2015. ScbR and ScbR2-mediated signal transduction networks coordinate complex physiological responses in Streptomyces coelicolor. Sci Rep 5:14831. https://doi.org/10.1038/srep14831.
33. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. https://doi.org/10.1186/1471-2105-5-113.
34. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029.
35. Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163. https://doi.org/10.1093/bib/5.2.150.
36. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426. https://doi.org/10.1093/oxfordjournals.molbev.a040410.
37. Jukes TH, Cantor CR. 1969. Evolution of protein molecules, p 21–132. In Munro HN (ed), Mammalian protein metabolism, vol 3. Academic Press, New York, NY.
38. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
39. Gust B, Challis GL, Fowler K, Kieser T, Chater KF. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100:1541–1546. https://doi.org/10.1073/pnas.0337542100.
40. Fernández-Martínez LT, Del Sol R, Evans MC, Fielding S, Herron PR, Chandra G, Dyson PJ. 2011. A transposon insertion single-gene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3(2). Antonie Van Leeuwenhoek 99:515–522. https:// doi.org/10.1007/s10482-010-9518-1.
41. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008. https://doi.org/10.1038/msb4100050.
42. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640– 6645. https://doi.org/10.1073/pnas.120163297.
43. Bergmeyer HU, Gawehn K, Grassl M. 1974. Enzymatic assay of pyruvate kinase, p 509–510. In Bergmeyer HU (ed), Methods of enzymatic analysis, 2nd ed, vol 1. Academic Press, New York, NY.
44. Lenski RE, Rose MR, Simpson SC, Tadler SC. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138:1315–1341. https://doi.org/10.1086/285289.