Inferring gene function from evolutionary change in signatures of translation efficiency

Genome Biology

Volumn 15, Issue 3, 2014, Pages

  Krisko, Anita ^a   Copic, Tea ^a   Gabaldón, Toni ^b,c,d   Lehner, Ben ^b,c,d   Supek, Fran ^b,c  

^a Mediterranean Institute for Life Sciences   (Croatia)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; IRON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSCRIPTOME;

AEROBE; ARCHAEAL GENOME; ARTICLE; BACTERIAL GENOME; CODON USAGE; CONTROLLED STUDY; ESCHERICHIA COLI; EVOLUTION; GENE FUNCTION; GENETIC VARIABILITY; HALOPHILE; HEAT TOLERANCE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PHYLOGENY; RNA TRANSLATION; SALT TOLERANCE; THERMOPHILE; ADAPTATION; ARCHAEAL GENE; ARCHAEON; BACTERIA; BACTERIAL GENE; GENETIC CODE; GENETICS; MOLECULAR EVOLUTION; PROTEIN SYNTHESIS;

ADAPTATION, PHYSIOLOGICAL; ARCHAEA; BACTERIA; EVOLUTION, MOLECULAR; GENES, ARCHAEAL; GENES, BACTERIAL; GENETIC CODE; PROTEIN BIOSYNTHESIS; TRANSCRIPTOME;

EID: 84899077335     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-3-r44     Document Type: Article

References (70)

1. Akashi H. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 1994, 136:927-935. 1205897, 8005445.
2. Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics 1991, 129:897-907. 1204756, 1752426.
3. Kanaya S, Yamada Y, Kudo Y, Ikemura T. Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 1999, 238:143-155. 10.1016/S0378-1119(99)00225-5, 10570992.
4. Sharp PM, Li WH. The Codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987, 15:1281-1295. 10.1093/nar/15.3.1281, 340524, 3547335.
5. Supek F, Vlahovicek K. Comparison of codon usage measures and their applicability in prediction of microbial gene expressivity. BMC Bioinformatics 2005, 6:182. 10.1186/1471-2105-6-182, 1199580, 16029499.
6. Welch M, Govindarajan S, Ness JE, Villalobos A, Gurney A, Minshull J, Gustafsson C. Design parameters to control synthetic gene expression in Escherichia coli. PLoS ONE 2009, 4:e7002. 10.1371/journal.pone.0007002, 2736378, 19759823.
7. Supek F, Smuc T. On relevance of codon usage to expression of synthetic and natural genes in Escherichia coli. Genetics 2010, 185:1129-1134. 10.1534/genetics.110.115477, 2900969, 20421604.
8. Rocha EPC. Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 2004, 14:2279-2286. 10.1101/gr.2896904, 525687, 15479947.
9. Supek F, Škunca N, Repar J, Vlahoviček K, Šmuc T. Translational selection is ubiquitous in prokaryotes. PLoS Genet 2010, 6:e1001004. 10.1371/journal.pgen.1001004, 2891978, 20585573.
10. Hershberg R, Petrov DA. General rules for optimal codon choice. PLoS Genet 2009, 5:e1000556. 10.1371/journal.pgen.1000556, 2700274, 19593368.
11. Drummond DA, Wilke CO. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 2008, 134:341-352. 10.1016/j.cell.2008.05.042, 2696314, 18662548.
12. Von Mandach C, Merkl R. Genes optimized by evolution for accurate and fast translation encode in Archaea and Bacteria a broad and characteristic spectrum of protein functions. BMC Genomics 2010, 11:617. 10.1186/1471-2164-11-617, 3091758, 21050470.
13. Karlin S, Brocchieri L, Mrázek J, Kaiser D. Distinguishing features of δ-proteobacterial genomes. Proc Natl Acad Sci 2006, 103:11352-11357. 10.1073/pnas.0604311103, 1544090, 16844781.
14. Carbone A. Computational prediction of genomic functional cores specific to different microbes. J Mol Evol 2006, 63:733-746. 10.1007/s00239-005-0250-9, 17103060.
15. Karlin S, Brocchieri L, Campbell A, Cyert M, Mrázek J. Genomic and proteomic comparisons between bacterial and archaeal genomes and related comparisons with the yeast and fly genomes. Proc Natl Acad Sci USA 2005, 102:7309-7314. 10.1073/pnas.0502314102, 1129125, 15883367.
16. Man O, Pilpel Y. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat Genet 2007, 39:415-421. 10.1038/ng1967, 17277776.
17. Grocock RJ, Sharp PM. Synonymous codon usage in Pseudomonas aeruginosa PA01. Gene 2002, 289:131-139. 10.1016/S0378-1119(02)00503-6, 12036591.
18. Retchless AC, Lawrence JG. Quantification of codon selection for comparative bacterial genomics. BMC Genomics 2011, 12:374. 10.1186/1471-2164-12-374, 3162537, 21787402.
19. Knight RD, Freeland SJ, Landweber LF. A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol 2001, 2:RESEARCH0010. 31479, 11305938.
20. Chen SL, Lee W, Hottes AK, Shapiro L, McAdams HH. Codon usage between genomes is constrained by genome-wide mutational processes. Proc Natl Acad Sci USA 2004, 101:3480-3485. 10.1073/pnas.0307827100, 373487, 14990797.
21. Dos Reis M, Savva R, Wernisch L. Solving the riddle of codon usage preferences: a test for translational selection. Nucl Acids Res 2004, 32:5036-5044. 10.1093/nar/gkh834, 521650, 15448185.
22. Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE. Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 2005, 33:1141-1153. 10.1093/nar/gki242, 549432, 15728743.
23. Carbone A, Képès F, Zinovyev A. Codon bias signatures, organization of microorganisms in codon space, and lifestyle. Mol Biol Evol 2005, 22:547-561.
24. Wagner A. Inferring lifestyle from gene expression patterns. Mol Biol Evol 2000, 17:1985-1987. 10.1093/oxfordjournals.molbev.a026299, 11110914.
25. Kudla G, Murray AW, Tollervey D, Plotkin JB. Coding-sequence determinants of gene expression in Escherichia coli. Science 2009, 324:255-258. 10.1126/science.1170160, 3902468, 19359587.
26. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 2003, 4:41. 10.1186/1471-2105-4-41, 222959, 12969510.
27. Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L. A role for tRNA modifications in genome structure and codon usage. Cell 2012, 149:202-213. 10.1016/j.cell.2012.01.050, 22464330.
28. Saini A, Mapolelo DT, Chahal HK, Johnson MK, Outten FW. SufD and SufC ATPase activity are required for iron acquisition during in vivo Fe-S cluster formation on SufB. Biochemistry 2010, 49:9402-9412. 10.1021/bi1011546, 3004146, 20857974.
29. Tokumoto U, Kitamura S, Fukuyama K, Takahashi Y. Interchangeability and distinct properties of bacterial Fe-S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J Biochem 2004, 136:199-209. 10.1093/jb/mvh104, 15496591.
30. Nachin L, El Hassouni M, Loiseau L, Expert D, Barras F, Nachin L, El Hassouni M, Loiseau L, Expert D, Barras F. SoxR-dependent response to oxidative stress and virulence of Erwinia chrysanthemi: the key role of SufC, an orphan ABC ATPase, SoxR-dependent response to oxidative stress and virulence of Erwinia chrysanthemi: the key role of SufC, an orphan ABC ATPase. Mol Microbiol, Mol Microbiol 2001, 39:960-972.
31. Loughlin MF, Arandhara V, Okolie C, Aldsworth TG, Jenks PJ. Helicobacter pylori mutants defective in the clpP ATP-dependant protease and the chaperone clpA display reduced macrophage and murine survival. Microb Pathog 2009, 46:53-57. 10.1016/j.micpath.2008.10.004, 18992803.
32. Ekaza E, Teyssier J, Ouahrani-Bettache S, Liautard J-P, Köhler S. Characterization of Brucella suis clpB and clpAB mutants and participation of the genes in stress responses. J Bacteriol 2001, 183:2677-2681. 10.1128/JB.183.8.2677-2681.2001, 95187, 11274130.
33. Chaturvedi R, Bansal K, Narayana Y, Kapoor N, Sukumar N, Togarsimalemath SK, Chandra N, Mishra S, Ajitkumar P, Joshi B, Katoch VM, Patil SA, Balaji KN. The multifunctional PE_PGRS11 protein from Mycobacterium tuberculosis plays a role in regulating resistance to oxidative stress. J Biol Chem 2010, 285:30389-30403. 10.1074/jbc.M110.135251, 2945531, 20558725.
34. Lee SM, Koh H-J, Park D-C, Song BJ, Huh T-L, Park J-W. Cytosolic NADP + -dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med 2002, 32:1185-1196. 10.1016/S0891-5849(02)00815-8, 12031902.
35. Kondoh H, Lleonart ME, Gil J, Wang J, Degan P, Peters G, Martinez D, Carnero A, Beach D. Glycolytic enzymes can modulate cellular life span. Cancer Res 2005, 65:177-185.
36. Cunningham L, Georgellis D, Green J, Guest JR. Co-regulation of lipoamide dehydrogenase and 2-oxoglutarate dehydrogenase synthesis in Escherichia coli: characterisation of an ArcA binding site in the lpd promoter. FEMS Microbiol Lett 1998, 169:403-408. 10.1111/j.1574-6968.1998.tb13347.x, 9868788.
37. Brown SD, Thompson MR, VerBerkmoes NC, Chourey K, Shah M, Zhou J, Hettich RL, Thompson DK. Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol Cell Proteomics 2006, 5:1054-1071. 10.1074/mcp.M500394-MCP200, 16524964.
38. Pinto R, Tang QX, Britton WJ, Leyh TS, Triccas JA. The Mycobacterium tuberculosis cysD and cysNC genes form a stress-induced operon that encodes a tri-functional sulfate-activating complex. Microbiology 2004, 150:1681-1686. 10.1099/mic.0.26894-0, 15184554.
39. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011, 39:D561-D568. 10.1093/nar/gkq973, 3013807, 21045058.
40. Blank L, Green J, Guest JR. AcnC of Escherichia coli is a 2-methylcitrate dehydratase (PrpD) that can use citrate and isocitrate as substrates. Microbiology 2002, 148:133-146.
41. Tang Y, Quail MA, Artymiuk PJ, Guest JR, Green J. Escherichia coli aconitases and oxidative stress: post-transcriptional regulation of sodA expression. Microbiology 2002, 148:1027-1037.
42. Ritz D, Beckwith J. Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 2001, 55:21-48. 10.1146/annurev.micro.55.1.21, 11544348.
43. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li S-MW, Kemner KM, Fredrickson JK. Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 2007, 5:e92. 10.1371/journal.pbio.0050092, 1828145, 17373858.
44. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes HM, Makarova KS, Wackett LP, Fredrickson JK, Ghosal D. Accumulation of Mn(II) in deinococcus radiodurans facilitates gamma-radiation resistance. Science 2004, 306:1025-1028. 10.1126/science.1103185, 15459345.
45. Singh R, Mailloux RJ, Puiseux-Dao S, Appanna VD. Oxidative stress evokes a metabolic adaptation that favors increased NADPH synthesis and decreased NADH production in Pseudomonas fluorescens. J Bacteriol 2007, 189:6665-6675. 10.1128/JB.00555-07, 2045160, 17573472.
46. Sandoval JM, Arenas FA, Vásquez CC. Glucose-6-phosphate dehydrogenase protects Escherichia coli from tellurite-mediated oxidative stress. PLoS ONE 2011, 6:e25573. 10.1371/journal.pone.0025573, 3184162, 21984934.
47. Grose JH, Joss L, Velick SF, Roth JR. Evidence that feedback inhibition of NAD kinase controls responses to oxidative stress. Proc Natl Acad Sci USA 2006, 103:7601-7606. 10.1073/pnas.0602494103, 1472491, 16682646.
48. Dougan DA, Reid BG, Horwich AL, Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol Cell 2002, 9:673-683. 10.1016/S1097-2765(02)00485-9, 11931773.
49. du Plessis L, Škunca N, Dessimoz C. The what, where, how and why of gene ontology-a primer for bioinformaticians. Brief Bioinform 2011, 12:723-735. 10.1093/bib/bbr002, 3220872, 21330331.
50. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci USA 1999, 96:4285-4288. 10.1073/pnas.96.8.4285, 16324, 10200254.
51. Korbel JO, Doerks T, Jensen LJ, Perez-Iratxeta C, Kaczanowski S, Hooper SD, Andrade MA, Bork P. Systematic association of genes to phenotypes by genome and literature mining. PLoS Biol 2005, 3:e134. 10.1371/journal.pbio.0030134, 1073694, 15799710.
52. Koonin EV, Wolf YI. Genomics of Bacteria and Archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 2008, 36:6688-6719. 10.1093/nar/gkn668, 2588523, 18948295.
53. Škunca N, Bošnjak M, Kriško A, Panov P, Džeroski S, Šmuc T, Supek F. Phyletic profiling with cliques of orthologs is enhanced by signatures of paralogy relationships. PLoS Comput Biol 2013, 9:e1002852. 10.1371/journal.pcbi.1002852, 3536626, 23308060.
54. Retchless AC, Lawrence JG. Ecological adaptation in bacteria: speciation driven by codon selection. Mol Biol Evol 2012, 29:3669-3683. 10.1093/molbev/mss171, 3494267, 22740635.
55. Botzman M, Margalit H. Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol 2011, 12:R109. 10.1186/gb-2011-12-10-r109, 3333779, 22032172.
56. Gabaldón T. Comparative genomics-based prediction of protein function. Methods Mol Biol 2008, 439:387-401. 10.1007/978-1-59745-188-8_26, 18370117.
57. Rui B, Shen T, Zhou H, Liu J, Chen J, Pan X, Liu H, Wu J, Zheng H, Shi Y. A systematic investigation of Escherichia coli central carbon metabolism in response to superoxide stress. BMC Syst Biol 2010, 4:122. 10.1186/1752-0509-4-122, 2944137, 20809933.
58. Singh R, Lemire J, Mailloux RJ, Appanna VD. A novel strategy involved anti-oxidative defense: the conversion of NADH into NADPH by a metabolic network. PLoS ONE 2008, 3:e2682. 10.1371/journal.pone.0002682, 2443280, 18628998.
59. NCBI Entrez Genome FTP site ftp://ftp.ncbi.nih.gov/genomes/Bacteria.
60. Breiman L. Random forests. Mach Learn 2001, 45:5-32.
61. NCBI Entrez Microbial Genome Properties http://www.ncbi.nlm.nih.gov/genome/browse/, NCBI Entrez Microbial Genome Properties.
62. Fawcett T. An introduction to ROC analysis. Pattern Recogn Lett 2006, 27:861-874.
63. The FastRandomForest Weka Extension http://fast-random-forest.googlecode.com/, The FastRandomForest Weka Extension.
64. Witten IH, Frank E. Practical Machine Learning Tools and Techniques, Second Edition 2005, San Francisco: Morgan Kaufmann, 2.
65. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. Complete Set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 2006, 12:291-299.
66. Zhang W, O'Connor K, Wang DIC, Li Z. Bioreduction with efficient recycling of NADPH by coupled permeabilized microorganisms. Appl Environ Microbiol 2009, 75:687-694. 10.1128/AEM.01506-08, 2632151, 19047388.
67. Rad AM, Janic B, Iskander ASM, Soltanian-Zadeh H, Arbab AS. Measurement of quantity of iron in magnetically labeled cells: comparison among different UV/VIS spectrometric methods. Biotechniques 2007, 43:627-628. 630, 632 passim, 10.2144/000112599, 18072592.
68. Markham NR, Zuker M. UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 2008, 453:3-31. 10.1007/978-1-60327-429-6_1, 18712296.
69. Shultzaberger RK, Bucheimer RE, Rudd KE, Schneider TD. Anatomy of Escherichia coli ribosome binding sites. J Mol Biol 2001, 313:215-228. 10.1006/jmbi.2001.5040, 11601857.
70. Karlin S, Mrazek J. Predicted highly expressed genes of diverse prokaryotic genomes. J Bacteriol 2000, 182:5238-5250. 10.1128/JB.182.18.5238-5250.2000, 94675, 10960111.