The slow:fast substitution ratio reveals changing patterns of natural selection in γ-proteobacterial genomes

ISME Journal

Volumn 3, Issue 10, 2009, Pages 1180-1192

  Shapiro, B Jesse ^a   Alm, Eric ^a,b,c,d  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c Virtual Institute of Microbial Stress and Survival   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

Comparative genomics; Ecological adaptation; G proteobacteria; Positive selection; Reverse ecology

Indexed keywords

BACTERIAL DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BIOLOGY; CLUSTER ANALYSIS; GAMMAPROTEOBACTERIA; GENETIC SELECTION; GENETICS; METHODOLOGY; MOLECULAR EVOLUTION; MUTATION;

CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GAMMAPROTEOBACTERIA; GENES, BACTERIAL; GENOME, BACTERIAL; MUTATION; SELECTION (GENETICS);

BACTERIA (MICROORGANISMS); BUCHNERA (PROTEOBACTERIA); PROTEOBACTERIA; PSEUDOMONAS FLUORESCENS;

EID: 70349459568     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2009.51     Document Type: Article

References (50)

1. Alm EJ, Huang KH, Price MN, Koche RP, Keller K, Dubchak IL et al. (2005). The MicrobesOnline web site for comparative genomics. Genome Res 15: 1015-1022.
2. Arjunan P, Nemeria N, Brunskill A, Chandrasekhar K, Sax M, Yan Y et al. (2002). Structure of the pyruvate dehydrogenase multienzyme complex E1 component from Escherichia coli at 1.85A° resolution. Biochemistry 41: 5213-5221.
3. Astuti D, Latif F, Dallol A, Dahia PL, Douglas F, George E et al. (2001). Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet 69: 49-54.
4. Clamp M, Cuff J, Searle SM, Barton GJ. (2004). The Jalview Java alignment editor. Bioinformatics 20: 426-427.
5. Das M, Chopra AK, Cantu JM, Peterson JW. (1998). Antisera to selected outer membrane proteins of Vibrio cholerae protect against challenge with homologous and heterologous strains of V. cholerae. FEMS Immunol Med Microbiol 22: 303-308.
6. DeLano WL. (2002). The PyMOL Molecular Graphics System http://www.pymol.org/.
7. Falush D, Bowden R. (2006). Genome-wide association mapping in bacteria? Trends Microbiol 14: 353-355.
8. Fry AJ, Wernegreen JJ. (2005). The roles of positive and negative selection in the molecular evolution of insect endosymbionts. Gene 355: 1-10.
9. Guindon S, Gascuel O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
10. Guttman DS, Gropp SJ, Morgan RL, Wang PW. (2006). Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Mol Biol Evol 23: 2342-2354.
11. Herbeck JT, Funk DJ, Degnan PH, Wernegreen JJ. (2003). A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: Slightly deleterious mutations in the chaperonin groEL. Genetics 165: 1651-1660.
12. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I et al. (2008). High-throughput sequencing provides insights into genome variation and evolution in Salmonella typhi. Nat Genet 40: 987-993.
13. Hong H, Patel DR, Tamm LK, van den Berg B. (2006). The outer membrane protein OmpW forms an eightstranded beta-barrel with a hydrophobic channel. J Biol Chem 281: 7568-7577.
14. Hughes AL, Friedman R, Rivailler P, French JO. (2008). Synonymous and nonsynonymous polymorphisms versus divergences in bacterial genomes. Mol Biol Evol 25: 2199-2209.
15. Hughes AL. (2007). Looking for Darwin in all the wrong places: The misguided quest for positive selection at the nucleotide sequence level. Heredity 99: 364-373.
16. Hughes AL, Nei M. (1988). Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167-170.
17. Ishii N, Fujii M, Hartman PS, Tsuda M, Yasuda K, Senoo- Matsuda N et al. (1998). A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394: 694-697.
18. Itoh T, Martin W, Nei M. (2002). Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc Natl Acad Sci 99: 12944-12948.
19. Jordan IK, Kondrashov FA, Rogozin IB, Tatusov RL, Wolf YI, Koonin EV. (2001). Constant relative rate of protein evolution and detection of functional diversification among bacterial, archaeal and eukaryotic proteins. Genome Biol 2: RESEARCH0053.
20. Kimura M. (1977). Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267: 275-276.
21. Kryazhimskiy S, Plotkin JB. (2008). The population genetics of dN/dS. PLoS Genet 4: e1000304.
22. Li YF, Costello JC, Holloway AK, Hahn MW. (2008). 'Reverse ecology' and the power of population genomics. Evolution 62: 2984-2994.
23. MaW, Dong FF, Stavrinides J, Guttman DS. (2006). Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet 2: e209.
24. Massingham T, Goldman N. (2005). Detecting amino acid sites under positive selection and purifying selection. Genetics 169: 1753-1762.
25. Mavrodi DV, Blankenfeldt W, Thomashow LS. (2006). Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44: 417-445.
26. Moran NA. (1996). Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci 93: 2873-2878.
27. Nei M, Gojobori T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
28. Nei M, Kumar S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press: Oxford, UK.
29. Nozawa M, Suzuki Y, Nei M. (2009). Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci (doi: 10.1073/pnas.0901855106, early edition).
30. Ochman H, Elwyn S, Moran NA. (1999). Calibrating bacterial evolution. Proc Natl Acad Sci USA 96: 12638-12643.
31. Paulsen IT, Press CM, Ravel J, Kobayashi DY, Myers GS, Mavrodi DV et al. (2005). Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf- 5. Nat Biotechnol 23: 873-878.
32. Price MN, Arkin AP, Alm EJ. (2006). OpWise: Operons aid the identification of differentially expressed genes in bacterial microarray experiments. BMC Bioinformatics 7: 19.
33. Price-Whelan A, Dietrich LE, Newman DK. (2007). Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J Bacteriol 189: 6372-6381.
34. Price-Whelan A, Dietrich LE, Newman DK. (2006). Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2: 71-78.
35. Pupko T, Pe'er I, Shamir R, Graur D. (2000). A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol Biol Evol 17: 890-896.
36. Rocha EP, Smith JM, Hurst LD, Holden MT, Cooper JE, Smith NH et al. (2006). Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239: 226-235.
37. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ, Schaffner SF et al. (2002). Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832-837.
38. Shapiro BJ, Alm EJ. (2008). Comparing patterns of natural selection across species using selective signatures. PLoS Genet 4: e23.
39. Shapiro BJ, David LA, Friedman J, Alm EJ. (2009). Looking for Darwin's footprints in the microbial world. Trends Microbiol 17: 5 (in press).
40. Sokurenko EV, Feldgarden M, Trintchina E, Weissman SJ, Avagyan S, Chattopadhyay S et al. (2004). Selection footprint in the FimH adhesin shows pathoadaptive niche differentiation in Escherichia coli. Mol Biol Evol 21: 1373-1383.
41. Storey JD, Tibshirani R. (2003). Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445.
42. Tatusov RL, Koonin EV, Lipman DJ. (1997). A genomic perspective on protein families. Science 278: 631-637.
43. Weber E, Koebnik R. (2006). Positive selection of the Hrp pilin HrpE of the plant pathogen Xanthomonas. J Bacteriol 188: 1405-1410.
44. Woolfit M, Bromham L. (2003). Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol Biol Evol 20: 1545-1555.
45. Xu C, Wang S, Ren H, Lin X, Wu L, Peng X. (2005). Proteomic analysis on the expression of outer membrane proteins of Vibrio alginolyticus at different sodium concentrations. Proteomics 5: 3142-3152.
46. Yang Z, Nielsen R. (2002). Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19: 908-917.
47. Yang Z. (1998). Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15: 568-573.
48. Yang Z. (1997). PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
49. Yankovskaya V, Horsefield R, Tornroth S, Luna-Chavez C, Miyoshi H, Leger C et al. (2003). Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299: 700-704.
50. Zeng K, Fu YX, Shi S, Wu CI. (2006). Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174: 1431-1439.