Duplication and evolution of devA-like genes in Streptomyces has resulted in distinct developmental roles

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Clark, Laura C ^a   Hoskisson, Paul A ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOBACTERIA; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; CLADISTICS; CONTROLLED STUDY; DEVA GENE; DEVA LIKE GENE; DEVE GENE; DNA BINDING; ENZYME SPECIFICITY; GENE DISRUPTION; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENETIC COMPLEMENTATION; GENETIC VARIABILITY; LIFE CYCLE; MICROBIAL MORPHOLOGY; MOLECULAR EVOLUTION; MYCELIUM; NONHUMAN; OLIGOMERIZATION; PARALOGY; PHENOTYPE; REGULATOR GENE; SALINOSPORA; SPOROGENESIS; STREPTOMYCES; STREPTOMYCES COELICOLOR; ACTINOMYCES; BACTERIAL CHROMOSOME; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); POSIBACTERIA; SALINISPORA; STREPTOMYCES; STREPTOMYCES COELICOLOR;

BACTERIAL PROTEIN; TRANSCRIPTION FACTOR;

ACTINOMYCES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, NUCLEIC ACID; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS;

EID: 80053605436     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025049     Document Type: Article

References (57)

1. Karandikar A, Sharples GP, Hobbs G, (1997) Differentiation of Streptomyces coelicolor A3(2) under nitrate-limited conditions. Microbiology 143: 3581-3590.
2. Flardh K, Buttner MJ, (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
3. Elliot MA, Talbot NJ, (2004) Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr Opin Microbiol 7: 594-601.
4. Nodwell JR, McGovern K, Losick R, (1996) An oligopeptide permease responsible for the import of an extracellular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol Microbiol 22: 881-893.
5. Nodwell JR, Yang M, Kuo D, Losick R, (1999) Extracellular complementation and the identification of additional genes involved in aerial mycelium formation in Streptomyces coelicolor. Genetics 151: 569-584.
6. Willey JM, Willems A, Kodani S, Nodwell JR, (2006) Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol Microbiol 59: 731-742.
7. Chater KF, (2001) Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex? Curr Opin Microbiol 4: 667-673.
8. Chater KF, Chandra G, (2006) The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol Rev 30: 651-672.
9. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, et al. (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71: 495-548.
10. Bergthorsson U, Andersson DI, Roth JR, (2007) Ohno's dilemma: evolution of new genes under continuous selection. Proc Natl Acad Sci U S A 104: 17004-17009.
11. Claessen D, Wosten HA, van Keulen G, Faber OG, Alves AM, et al. (2002) Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol Microbiol 44: 1483-1492.
12. Claessen D, Rink R, de Jong W, Siebring J, de Vreugd P, et al. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17: 1714-1726.
13. Elliot MA, Karoonuthaisiri N, Huang J, Bibb MJ, Cohen SN, et al. (2003) The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev 17: 1727-1740.
14. 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.
15. Andersson DI, Hughes D, (2009) Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43: 167-195.
16. Thomaides HB, Davison EJ, Burston L, Johnson H, Brown DR, et al. (2007) Essential bacterial functions encoded by gene pairs. J Bacteriol 189: 591-602.
17. Treangen TJ, Rocha EP, (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7: e1001284.
18. Teichmann SA, Babu MM, (2004) Gene regulatory network growth by duplication. Nat Genet 36: 492-496.
19. Ohno S, (1970) Evolution by gene duplication: Springer-Verlag.
20. Lynch M, Force A, (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
21. Huminiecki L, Wolfe KH, (2004) Divergence of spatial gene expression profiles following species-specific gene duplications in human and mouse. Genome Res 14: 1870-1879.
22. He X, Zhang J, (2005) Gene complexity and gene duplicability. Curr Biol 15: 1016-1021.
23. Goldman BS, Nierman WC, Kaiser D, Slater SC, Durkin AS, et al. (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103: 15200-15205.
24. Hoskisson PA, Rigali S, Fowler K, Findlay KC, Buttner MJ, (2006) DevA, a GntR-like transcriptional regulator required for development in Streptomyces coelicolor. J Bacteriol 188: 5014-5023.
25. Hoskisson PA, Rigali S, (2009) Chapter 1: Variation in form and function the helix-turn-helix regulators of the GntR superfamily. Adv Appl Microbiol 69: 1-22.
26. Huang J, Shi J, Molle V, Sohlberg B, Weaver D, et al. (2005) Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol Microbiol 58: 1276-1287.
27. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
28. Haydon DJ, Guest JR, (1991) A new family of bacterial regulatory proteins. FEMS Microbiol Lett 63: 291-295.
29. Hillerich B, Westpheling J, (2006) A new GntR family transcriptional regulator in streptomyces coelicolor is required for morphogenesis and antibiotic production and controls transcription of an ABC transporter in response to carbon source. J Bacteriol 188: 7477-7487.
30. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, et al. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675.
31. Ryding NJ, Kelemen GH, Whatling CA, Flardh K, Buttner MJ, et al. (1998) A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol Microbiol 29: 343-357.
32. Sprusansky O, Zhou L, Jordan S, White J, Westpheling J, (2003) Identification of three new genes involved in morphogenesis and antibiotic production in Streptomyces coelicolor. J Bacteriol 185: 6147-6157.
33. Prud'homme B, Gompel N, Carroll SB, (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 (Suppl 1): 8605-8612.
34. Veening JW, Hamoen LW, Kuipers OP, (2005) Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis. Mol Microbiol 56: 1481-1494.
35. Stackebrandt E, Rainey FA, Ward-Rainey NL, (1997) Proposal for a new hierarchical classification system, Actinobacteria classis nov. Int J Syst Bacteriol 47: 479-491.
36. Campanaro S, Treu L, Valle G, (2008) Protein evolution in deep sea bacteria: an analysis of amino acids substitution rates. BMC Evol Biol 8: 313.
37. Nowak MA, Boerlijst MC, Cooke J, Smith JM, (1997) Evolution of genetic redundancy. Nature 388: 167-171.
38. Zhang J, (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18: 292-298.
39. Lynch M, Conery JS, (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
40. Johnson DA, Thomas MA, (2007) The monosaccharide transporter gene family in Arabidopsis and rice: a history of duplications, adaptive evolution, and functional divergence. Mol Biol Evol 24: 2412-2423.
41. Skamnioti P, Furlong RF, Gurr SJ, (2008) The fate of gene duplicates in the genomes of fungal pathogens. Commun Integr Biol 1: 196-198.
42. Skamnioti P, Furlong RF, Gurr SJ, (2008) Evolutionary history of the ancient cutinase family in five filamentous Ascomycetes reveals differential gene duplications and losses and in Magnaporthe grisea shows evidence of sub- and neo-functionalization. New Phytol 180: 711-721.
43. Hobbs G, Frazer CM, Gardner DCJ, Cullum JA, Oliver SG, (1989) Dispersed growth of Streptomyces in liquid culture. Appl Microbiol Biotechnol 31: 272-277.
44. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, et al. (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49.
45. Bishop A, Fielding S, Dyson P, Herron P, (2004) Systematic insertional mutagenesis of a streptomycete genome: a link between osmoadaptation and antibiotic production. Genome Res 14: 893-900.
46. 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.
47. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA, (2000) Practical Streptomyces genetics Norwich John Innes Foundation.
48. Kelemen GH, Brown GL, Kormanec J, Potuckova L, Chater KF, et al. (1996) The positions of the sigma-factor genes, whiG and sigF, in the hierarchy controlling the development of spore chains in the aerial hyphae of Streptomyces coelicolor A3(2). Mol Microbiol 21: 593-603.
49. Thompson JD, Gibson TJ, Higgins DG, (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2 3.
50. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
51. Nei M, Gojobori T, (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
52. Gregory MA, Till R, Smith MCM, (2003) Integration site for Streptomyces phage _BT1 and development of site-specific integrating vectors. J Bacteriol 185: 5320-5323.
53. Goodfellow M, Cross T, (1983) Classification. The Biology of the Actinomycetes Academic Press, London.
54. Maldonado LA, Fenical W, Jensen PR, Kauffman CA, Mincer TJ, et al. (2005) Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae. Int J Syst Evol Microbiol 55: 1759-1766.
55. Park YH, Yoon JH, Shin YK, Suzuki K, Kudo T, et al. (1999) Classification of 'Nocardioides fulvus' IFO 14399 and Nocardioides sp. ATCC 39419 in Kribbella gen. nov., as Kribbella flavida sp. nov. and Kribbella sandramycini sp. nov. Int J Syst Bacteriol 49: 743-52.
56. Labeda DP, Kroppenstedt RM, (2005) Stackebrandtia nassauensis gen. nov., sp. nov. and emended description of the family Glycomycetaceae. Int J Syst Evol Microbiol 55: 1687-91.
57. Hasegawa T, Lechevalier MP, Lechevalier HA, (1978) New Genus of the actinomycetales: Actinosynnema gen. nov. Int J Syst Bacteriol 28: 304-310.