Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Thakur, Subarna ^a   Normand, Philippe ^b   Daubin, Vincent ^c   Tisa, Louis S ^d   Sen, Arnab ^a  

^a UNIVERSITY OF NORTH BENGAL   (India)

^b University of Lyon   (France)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSITY OF NEW HAMPSHIRE   (United States)

Author keywords

Actinobacteria; Pathogenesis; Purifying selection; Secretome; Symbiosis

Indexed keywords

NON SECRETORY PROTEIN; PROTEOME; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ALDER; ANGIOSPERM; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATION; CASUARINACEAE; CODON USAGE; CONTROLLED STUDY; ELAEAGNACEAE; FRANKIA; GENE; GENE EXPRESSION; GENETIC VARIABILITY; GENOME ANALYSIS; MUTATION RATE; MYCOBACTERIUM; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM ULCERANS; MYRICACEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT PATHOGEN INTERACTION; PROTEIN SECRETION; RHAMNACEAE; SECRETORY PROTEIN GENE; SPECIES DIFFERENCE; STREPTOMYCES; STREPTOMYCES AVERMITILIS; STREPTOMYCES COELICOLOR; STREPTOMYCES GRISEUS; SYMBIONT;

ACTINOBACTERIA; CODON; EVOLUTION, MOLECULAR; PROTEOME; SELECTION, GENETIC;

ACTINOBACTERIA; ANIMALIA; EUKARYOTA; FRANKIA; MAMMALIA; MYCOBACTERIUM; STREPTOMYCES;

EID: 84880127354     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-474     Document Type: Article

References (56)

1. Benson DR, Silvester WB. Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 1993, 57(2):293-319. 372911, 8336669.
2. Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson J, Evtushenko L, Misra AK. Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 1996, 46(1):1-9. 10.1099/00207713-46-1-1, 8573482.
3. Normand P, Chapelon C. Direct characterization of Frankia and of close phyletic neighbors from an Alnus viridis rhizosphere. Physiol Plant 1997, 99:722-731.
4. Normand P. Geodermatophilaceae fam. nov., a formal description. Int J Syst Evol Microbiol 2006, 56:2277-2278. 10.1099/ijs.0.64298-0, 17012547.
5. Babalola OO, Kirby BM, Le Roes-Hill M, Cook AE, Cary SC, Burton SG, Cowan DA. Phylogenetic analysis of actinobacterial populations associated with Antarctic Dry Valley mineral soils. Environ Microbiol 2009, 11(3):566-576. 10.1111/j.1462-2920.2008.01809.x, 19278445.
6. Mort A, Normand P, Lalonde M. 2-O-methyl-D-mannose, a key sugar in the taxonomy of Frankia. Can J Microbiol 1983, 29:993-1002.
7. Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD. Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 1993, 90:6091-6094. 10.1073/pnas.90.13.6091, 46873, 11607408.
8. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, et al. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 2008, 105:4928-4932. 10.1073/pnas.0710618105, 2290763, 18316735.
9. Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, et al. Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 2011, 156:1-12.
10. Normand P, Queiroux C, Tisa LS, Benson DR, Cruveiller S, Rouy Z, Medigue C. Exploring the genomes of Frankia sp. Physiol Plant 2007, 13:331-343.
11. Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, et al. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 2007, 17(1):7-15. 1716269, 17151343.
12. Mastronunzio JE, Tisa LS, Normand P, Benson DR. Comparative secretome analysis suggests low plant cell wall degrading capacity in Frankia symbionts. BMC Genomics 2008, 9:47. 10.1186/1471-2164-9-47, 2266912, 18226217.
13. Alloisio N, Félix S, Maréchal J, Pujic P, Rouy Z, Vallenet D, Medigue C, Normand P. Frankia alni proteome under nitrogen-fixing and nitrogen-replete conditions. Physiol Plant 2007, 13:440-453.
14. Waksman SA, Reilly HC, Johnstone DB. Isolation of streptomycin-producing strains of Streptomyces griseus. J Bacteriol 1946, 52:393-397.
15. Bouchek-Mechiche K, Gardan L, Andrivon D, Normand P. Streptomyces turgidiscabies and Streptomyces reticuliscabiei: one genomic species, two pathogenic groups. Int J Syst Evol Microbiol 2006, 56(Pt 12):2771-2776.
16. Kirby R, Sangal V, Tucker NP, Zakrzewska-Czerwinska J, Wierzbicka K, Herron PR, Chu CJ, Chandra G, Fahal AH, Goodfellow M, et al. Draft genome sequence of the human pathogen Streptomyces somaliensis, a significant cause of actinomycetoma. J Bacteriol 2012, 194(13):3544-3545. 10.1128/JB.00534-12, 3434723, 22689234.
17. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393(6685):537-544. 10.1038/31159, 9634230.
18. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, et al. Massive gene decay in the leprosy bacillus. Nature 2001, 409(6823):1007-1011. 10.1038/35059006, 11234002.
19. Kweon O, Kim SJ, Jones RC, Freeman JP, Adjei MD, Edmondson RD, Cerniglia CE. A polyomic approach to elucidate the fluoranthene-degradative pathway in Mycobacterium vanbaalenii PYR-1. J Bacteriol 2007, 189(13):4635-4647. 10.1128/JB.00128-07, 1913438, 17449607.
20. Martino A, Sacchi A, Volpe E, Agrati C, De Santis R, Pucillo LP, Colizzi V, Vendetti S. Non-pathogenic Mycobacterium smegmatis induces the differentiation of human monocytes directly into fully mature dendritic cells. J Clin Immun 2005, 25(4):365-375. 10.1007/s10875-005-4188-x, 16133993.
21. Baron C, Zambryski PC. The plant response in pathogenesis, symbiosis, and wounding: variations on a common theme?. Ann Rev Genet 1995, 29:107-129. 10.1146/annurev.ge.29.120195.000543, 8825470.
22. Brown JK, Tellier A. Plant-parasite coevolution: bridging the gap between genetics and ecology. Ann Rev Phytopathol 2011, 49:345-367.
23. Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach AM, et al. Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ Microbiol 1999, 1(6):525-533. 10.1046/j.1462-2920.1999.00068.x, 11207774.
24. Alloisio N, Queiroux C, Fournier P, Pujic P, Normand P, Vallenet D, Médigue C, Yamaura M, Kakoi K, Kucho KI. The Frankia alni symbiotic transcriptome. Mol Plant Microb Interactions 2010, 23:593-607.
25. Stukenbrock EH, Jorgensen FG, Zala M, Hansen TT, McDonald BA, Schierup MH. Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genetics 2010, 6(12):e1001189. 10.1371/journal.pgen.1001189, 3009667, 21203495.
26. Gong X, Padhi A. Evidence for positive selection in the extracellular domain of human cytomegalovirus encoded G protein-coupled receptor US28. J Med Virol 2011, 83(7):1255-1261. 10.1002/jmv.22098, 21520142.
27. Huang Y, Temperley ND, Ren L, Smith J, Li N, Burt DW. Molecular evolution of the vertebrate TLR1 gene family-a complex history of gene duplication, gene conversion, positive selection and co-evolution. BMC Evol Biol 2011, 11:149. 10.1186/1471-2148-11-149, 3125219, 21619680.
28. Delport W, Scheffler K, Seoighe C. Frequent toggling between alternative amino acids is driven by selection in HIV-1. PLoS Pathogens 2008, 4(12):e1000242. 10.1371/journal.ppat.1000242, 2592544, 19096508.
29. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, Chintha R, Harzen A, Colby T, Kamoun S, van der Hoorn RA. Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 2008, 20(4):1169-1183. 10.1105/tpc.107.056325, 2390736, 18451324.
30. Bailly X, Olivieri I, De Mita S, Cleyet-Marel JC, Bena G. Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago. Molec Ecol 2006, 15(10):2719-2734.
31. Brownlie JC, Adamski M, Slatko B, McGraw EA. Diversifying selection and host adaptation in two endosymbiont genomes. BMC Evol Biol 2007, 7:68. 10.1186/1471-2148-7-68, 1868728, 17470297.
32. Baker D, Torrey J. The isolation and cultivation of actinomycetous root nodule endophytes. Symbiotic Nitrogen Fixation in the Management of Temperate Forests 1979, 38-56. Oregon State University: Forest Research Laboratory, JC Gordon CW, Perry DA, Corvallis OR.
33. Becking JH. Frankiaceae fam. nov. (Actinomycetales) with one new combination and six new species of the genus Frankia Brunchorst 1886, 174. Int J Syst Bacteriol 1970, 20:201-220.
34. Lancelle S, Torrey J, Hepler P, Callaham D. Ultrastructure of freeze-substituted Frankia strain HFPCcI3, the actinomycete isolated from root nodules of Casuarina cunninghamiana. Protoplasma 1985, 127:64-72.
35. Gauthier D, Diem H, Dommergues Y. In vitro nitrogen fixation by two actinomycete strains isolated from Casuarina nodules. Appl Environ Microbiol 1981, 41:306-308. 243679, 16345698.
36. Normand P, Lalonde M. Evaluation of Frankia strains isolated from provenances of two Alnus species. Can J Microbiol 1982, 28:1133-1142.
37. Smolander A, Ronkko R, Nurmiaho-Lassila E-L, Haahtela K. Growth of Frankia in the rhizosphere of Betula pendula, a nonhost tree species. Can J Microbiol 1990, 36:649-656.
38. Baker D, Newcomb W, Torrey JG. Characterization of an ineffective actinorhizal microsymbiont, Frankia sp. EuI1 (Actinomycetales). Can J Microbiol 1980, 26:1072-1089. 10.1139/m80-180, 7459722.
39. Cooper CR, Hanson LA, Diehl WJ, Pharr GT, Coats KS. Natural selection of the Pol gene of bovine immunodeficiency virus. Virology 1999, 255(2):294-301. 10.1006/viro.1998.9572, 10069955.
40. Waterston RH, Lander ES, Sulston JE. On the sequencing of the human genome. Proc Natl Acad Sci USA 2002, 99(6):3712-3716. 10.1073/pnas.042692499, 122589, 11880605.
41. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 2002, 12(6):962-968. 1383730, 12045149.
42. Bergelson J, Kreitman M, Stahl EA, Tian D. Evolutionary dynamics of plant R-genes. Science 2001, 292(5525):2281-2285. 10.1126/science.1061337, 11423651.
43. Schuffenecker I, Ando T, Thouvenot D, Lina B, Aymard M. Genetic classification of "Sapporo-like viruses". Arch Virol 2001, 146(11):2115-2132. 10.1007/s007050170024, 11765915.
44. Lan R, Lumb B, Ryan D, Reeves PR. Molecular evolution of large virulence plasmid in Shigella clones and enteroinvasive Escherichia coli. Inf Imm 2001, 69(10):6303-6309.
45. Shahsavandi S, Salmanian AH, Ghorashi SA, Masoudi S, Ebrahimi MM. Evolutionary characterization of hemagglutinin gene of H9N2 influenza viruses isolated from Asia. Res Vet Sci 2012, 93(1):234-239. 10.1016/j.rvsc.2011.07.033, 21907373.
46. Hegde RS. Targeting and beyond: new roles for old signal sequences. Molec Cell 2002, 10(4):697-698. 10.1016/S1097-2765(02)00692-5, 12419211.
47. Graur D, Li WH. Fundamentals of molecular evolution, vol. 2 2000, Sunderland, MA: , Associates S.
48. Li YD, Xie ZY, Du YL, Zhou Z, Mao XM, Lv LX, Li YQ. The rapid evolution of signal peptides is mainly caused by relaxed selection on non-synonymous and synonymous sites. Gene 2009, 436(1-2):8-11.
49. Buggiotti L, Primmer CR. Molecular evolution of the avian growth hormone gene and comparison with its mammalian counterpart. J Evol Biol 2006, 19(3):844-854. 10.1111/j.1420-9101.2005.01042.x, 16674581.
50. Gu Z, David L, Petrov D, Jones T, Davis RW, Steinmetz LM. Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2005, 102(4):1092-1097. 10.1073/pnas.0409159102, 545845, 15647350.
51. Li W, Wu J, Tao W, Zhao C, Wang Y, He X, Chandra G, Zhou X, Deng Z, Chater KF, et al. A genetic and bioinformatic analysis of Streptomyces coelicolor genes containing TTA codons, possible targets for regulation by a developmentally significant tRNA. FEMS Microbiol Lett 2007, 266(1):20-28. 10.1111/j.1574-6968.2006.00494.x, 17100986.
52. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Molec Biol 2004, 340(4):783-795. 10.1016/j.jmb.2004.05.028, 15223320.
53. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Molec Biol 2001, 305(3):567-580. 10.1006/jmbi.2000.4315, 11152613.
54. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Molec Biol Evol 2007, 24(8):1586-1591. 10.1093/molbev/msm088, 17483113.
55. Sharp PM, Li WH. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987, 15(3):1281-1295. 10.1093/nar/15.3.1281, 340524, 3547335.
56. Wu G, Culley DE, Zhang W. Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 2005, 151(Pt 7):2175-2187.