Natural selection for operons depends on genome size

Genome Biology and Evolution

Volumn 5, Issue 11, 2013, Pages 2242-2254

  Nuñez, Pablo A ^a   Romero, Héctor ^b   Farber, Marisa D ^a   Rocha, Eduardo P C ^c,d  

^a INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

Author keywords

Evolution; Operons; Prokaryotes

Indexed keywords

ESCHERICHIA COLI PROTEIN;

ARTICLE; ESCHERICHIA COLI; EVOLUTION; GENETIC SELECTION; GENETICS; GENOME SIZE; METABOLISM; MOLECULAR EVOLUTION; OPERON; OPERONS; PROKARYOTE;

EVOLUTION; OPERONS; PROKARYOTES;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; GENOME SIZE; OPERON; SELECTION, GENETIC;

EID: 84892664123     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt174     Document Type: Article

References (87)

1. Akashi H, Gojobori T. 2002. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci U S A. 99:3695-3700.
2. Allen TE, et al. 2003. Genome-scale analysis of the uses of the Escherichia coli genome: model-driven analysis of heterogeneous data sets. J Bacteriol. 185:6392-6399.
3. Andersson JO, Andersson SG. 2001. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol Biol Evol. 18:829-839.
4. Baba T, et al. 2006. Construction of Escherichia coli K-12 in-frame, singlegene knockout mutants: the Keio collection. Mol Syst Biol. 2. 2006.0008.
5. Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SG. 2004. Computational inference of scenarios for alpha-proteobacterial genome evolution. Proc Natl Acad Sci U S A. 101:9722-9727.
6. Brinza L, Calevro F, Duport G, Gaget K, Gautier C, Charles H. 2010. Structure and dynamics of the operon map of Buchnera aphidicola sp. strain APS. BMC Genomics 11:666.
7. Brouwer RW, Kuipers OP, van Hijum SA. 2008. The relative value of operon predictions. Brief Bioinform. 9:367-375.
8. Corbin RW, et al. 2003. Toward a protein profile of Escherichia coli: comparison to its transcription profile. Proc Natl Acad Sci U S A. 100:9232-9237.
9. Cordero OX, Hogeweg P. 2009. The impact of long-distance horizontal gene transfer on prokaryotic genome size. Proc Natl Acad Sci U S A. 106:21748-21753.
10. Covert MW, Knight EM, Reed JL, Herrgard MJ, Palsson BO. 2004. Integrating high-throughput and computational data elucidates bacterial networks. Nature 429:92-96.
11. Charoensawan V, Wilson D, Teichmann SA. 2013. Genomic repertoires of DNA-binding transcription factors across the tree of life. Nucleic Acids Res. 38:7364-7377.
12. Cherry JL. 2003. Genome size and operon content. J Theor Biol. 221:401-410.
13. Chuang LY, Chang HW, Tsai JH, Yang CH. 2012. Features for computational operon prediction in prokaryotes. Brief Funct Genomics. 11:291-299.
14. de Daruvar A, Collado-Vides J, Valencia A. 2002. Analysis of the cellular functions of Escherichia coli operons and their conservation in Bacillus subtilis. J Mol Evol. 55:211-221.
15. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461.
16. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297:1183-1186.
17. Erickson BW, Sellers PH. 1983. Recognition of patterns in genetic sequences. In: Sankoff D, Kruskal JB, editors. Time warps, string edits and macromolecules: the theory and practice of sequence comparison. Reading (MA): Addison Wesley. p. 55-91.
18. Fang G, Rocha EP, Danchin A. 2008. Persistence drives gene clustering in bacterial genomes. BMC Genomics 9:4.
19. Felsenstein J. 1985. Phylogenies and the comparative method. Am Naturalist 125:1-15.
20. Galperin MY. 2006. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol. 188:4169-4182.
21. Gogarten JP, Doolittle WF, Lawrence JG. 2002. Prokaryotic evolution in light of gene transfer. Mol Biol Evol. 19:2226-2238.
22. Gouy M, Gautier C. 1982. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 10:7055-7074.
23. Guell M, et al. 2009. Transcriptome complexity in a genome-reduced bacterium. Science 326:1268-1271.
24. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
25. Huynen M, Snel B, Lathe W 3rd, Bork P. 2000. Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res. 10:1204-1210.
26. Jacob F, Monod J. 1961. Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol. 3:318-356.
27. Kennemann L, et al. 2011. Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci U S A. 108:5033-5038.
28. Klasson L, Andersson SG. 2004. Evolution of minimal-gene-sets in hostdependent bacteria. Trends Microbiol. 12:37-43.
29. Koch A, Levy H. 1955. Protein turnover in growing cultures of Escherichia coli. J Biol Chem. 217:947-957.
30. Konstantinidis KT, Tiedje JM. 2004. Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci U S A. 101:3160-3165.
31. Kovacs K, Hurst LD, Papp B. 2009. Stochasticity in protein levels drives colinearity of gene order in metabolic operons of Escherichia coli. PLoS Biol. 7:e1000115.
32. Kuo CH, Moran NA, Ochman H. 2009. The consequences of genetic drift for bacterial genome complexity. Genome Res. 19:1450-1454.
33. Kvam PH, Vidakovic B. 2007. Nonparametric statistics with applications to science and engineering. Hoboken (NJ): John Wiley & Sons.
34. Lathe WC, Snel B, Bork P. 2000. Gene context conservation of a higher order than operons. Trends Biochem Sci. 25:474-479.
35. Lawrence JG. 2003. Gene organization: selection, selfishness, and serendipity. Annu Rev Microbiol. 57:419-440.
36. Lawrence JG, Hendrix RW, Casjens S. 2001. Where are the pseudogenes in bacterial genomes? Trends Microbiol. 9:535-540.
37. Lawrence JG, Roth JR. 1996. Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143:1843-1860.
38. Lopez-Campistrous A, et al. 2005. Localization, annotation, and comparison of the Escherichia coli K-12 proteome under two states of growth. Mol Cell Proteomics. 4:1205-1209.
39. Lovdok L, et al. 2009. Role of translational coupling in robustness of bacterial chemotaxis pathway. PLoS Biol. 7:e1000171.
40. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. 2007. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol. 25:117-124.
41. Lynch M. 2006. Streamlining and simplification of microbial genome architecture. Annu Rev Microbiol. 60:327-349.
42. Maier T, Guell M, Serrano L. 2009. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583:3966-3973.
43. Mao F, Dam P, Chou J, Olman V, Xu Y. 2009. DOOR: a database for prokaryotic operons. Nucleic Acids Res. 37:D459-D463.
44. Masuda T, Saito N, Tomita M, Ishihama Y. 2009. Unbiased quantitation of Escherichia coli membrane proteome using phase transfer surfactants. Mol Cell Proteomics. 8:2770-2777.
45. McCutcheon JP, von Dohlen CD. 2011. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol. 21:1366-1372.
46. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. 2005. The microbial pan-genome. Curr Opin Genet Dev. 15:589-594.
47. Minezaki Y, Homma K, Nishikawa K. 2005. Genome-wide survey of transcription factors in prokaryotes reveals many bacteria-specific families not found in archaea. DNA Res. 12:269-280.
48. Mira A, Ochman H, Moran NA. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17:589-596.
49. Moran NA. 2003. Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol. 6:512-518.
50. Moran NA, Mira A. 2001. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2: RESEARCH0054.
51. Moreno-Hagelsieb G, Janga SC. 2008. Operons and the effect of genome redundancy in deciphering functional relationships using phylogenetic profiles. Proteins 70:344-352.
52. Moya A, Gil R, Latorre A, Pereto J, Pilar Garcillan-Barcia M, de la Cruz F. 2009. Toward minimal bacterial cells: evolution vs. design. FEMS Microbiol Rev. 33:225-235.
53. Mushegian AR, Koonin EV. 1996. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci U S A. 93:10268-10273.
54. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304.
55. Omelchenko MV, Makarova KS, Wolf YI, Rogozin IB, Koonin EV. 2003. Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol. 4:R55.
56. Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N. 1999. The use of gene clusters to infer functional coupling. Proc Natl Acad Sci U S A. 96:2896-2901.
57. Pal C, Hurst LD. 2003. Evidence for co-evolution of gene order and recombination rate. Nat Genet. 33:392-395.
58. Pal C, Hurst LD. 2004. Evidence against the selfish operon theory. Trends Genet. 20:232-234.
59. Papp B, Pal C, Hurst LD. 2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194-197.
60. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
61. Price MN, Alm EJ, Arkin AP. 2005. Interruptions in gene expression drive highly expressed operons to the leading strand of DNA replication. Nucleic Acids Res. 33:3224-3234.
62. Price MN, Arkin AP, Alm EJ. 2006. The life-cycle of operons. PLoS Genet. 2:e96.
63. Price MN, Huang KH, Arkin AP, Alm EJ. 2005. Operon formation is driven by co-regulation and not by horizontal gene transfer. Genome Res. 15:809-819.
64. R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
65. Ray JC, Igoshin OA. 2012. Interplay of gene expression noise and ultrasensitive dynamics affects bacterial operon organization. PLoS Comput Biol. 8:e1002672.
66. Rocha EP. 2006a. Inference and analysis of the relative stability of bacterial chromosomes. Mol Biol Evol. 23:513-522.
67. Rocha EP. 2006. The quest for the universals of protein evolution. Trends Genet. 22:412-416.
68. Rocha EP, Danchin A. 2004. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol. 21:108-116.
69. Sabatti C, Rohlin L, Oh MK, Liao JC. 2002. Co-expression pattern from DNA microarray experiments as a tool for operon prediction. Nucleic Acids Res. 30:2886-2893.
70. Salgado H, Moreno-Hagelsieb G, Smith TF, Collado-Vides J. 2000. Operons in Escherichia coli: genomic analyses and predictions. Proc Natl Acad Sci U S A. 97:6652-6657.
71. Schneiker S, et al. 2007. Complete genome sequence of the myxobacterium Sorangium cellulosum. Nat Biotechnol. 25:1281-1289.
72. Selinger DW, Saxena RM, Cheung KJ, Church GM, Rosenow C. 2003. Global RNA half-life analysis in Escherichia coli reveals positional patterns of transcript degradation. Genome Res. 13:216-223.
73. Sneppen K, Pedersen S, Krishna S, Dodd I, Semsey S. 2010. Economy of operon formation: cotranscription minimizes shortfall in protein complexes. MBio 1: pii:e00177-10.
74. Stahl FW, Murray NE. 1966. The evolution of gene clusters and genetic circularity in microorganisms. Genetics 53:569-576.
75. Swain PS. 2004. Efficient attenuation of stochasticity in gene expression through post-transcriptional control. J Mol Biol. 344:965-976.
76. Swain PS, Elowitz MB, Siggia ED. 2002. Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc Natl Acad Sci U S A. 99:12795-12800.
77. Taboada B, Ciria R, Martinez-Guerrero CE, Merino E. 2012. ProOpDB: Prokaryotic Operon DataBase. Nucleic Acids Res. 40:D627-D631.
78. Touchon M, Rocha EP. 2007. Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol. 24:969-981.
79. Treangen TJ, Rocha E. 2011. Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet. 7:e1001284.
80. van Nimwegen E. 2003. Scaling laws in the functional content of genomes. Trends Genet. 19:479-484.
81. Veitia RA. 2004. Gene dosage balance in cellular pathways: implications for dominance and gene duplicability. Genetics 168:569-574.
82. Vos P, et al. 2009. Bergey's manual of systematic bacteriology. New York: Springer.
83. Wang Z, Zhang J. 2011. Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc Natl Acad Sci U S A. 108:E67-E76.
84. Yin Y, Zhang H, Olman V, Xu Y. 2010. Genomic arrangement of bacterial operons is constrained by biological pathways encoded in the genome. Proc Natl Acad Sci U S A. 107:6310-6315.
85. Yus E, et al. 2009. Impact of genome reduction on bacterial metabolism and its regulation. Science 326:1263-1268.
86. Zaslaver A, Mayo A, Ronen M, Alon U. 2006. Optimal gene partition into operons correlates with gene functional order. Phys Biol. 3:183-189.
87. Zheng Y, Szustakowski JD, Fortnow L, Roberts RJ, Kasif S. 2002. Computational identification of operons in microbial genomes. Genome Res. 12:1221-1230.