Patterns of evolutionary conservation of essential genes correlate with their compensability

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Bergmiller, Tobias ^a,b,d   Ackermann, Martin ^a,b   Silander, Olin K ^a,b,c  

^a ETH ZURICH   (Switzerland)

^b Department of Environmental Microbiology ^*  (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; FERRITIN; PERIPLASMIC PROTEIN; PHOSPHATIDYLSERINE SYNTHASE; SERINE PROTEINASE;

ARTICLE; BACTERIAL GENETICS; BACTERIUM MUTANT; COLONY FORMATION; CONTROLLED STUDY; DEGP GENE; DEGS GENE; DPIA GENE; ESCHERICHIA COLI; ESSENTIAL GENE; FTNA GENE; FTSK GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE ISOLATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC MANIPULATION; HIGH COPY SUPPRESSOR GENE; IPSU GENE; LOLA GENE; NONHUMAN; NRDAB GENE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PSSA GENE; RHO GENE; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; SUPPRESSOR GENE; YCIR GENE; YGJD GENE; YHBJ GENE; BACTERIAL GENOME; GENE INACTIVATION; GENETICS; MOLECULAR EVOLUTION; MUTATION; STRUCTURAL HOMOLOGY;

ESCHERICHIA COLI;

CONSERVED SEQUENCE; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; GENES, ESSENTIAL; GENOME, BACTERIAL; MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84864052594     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002803     Document Type: Article

References (70)

1. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology 2: 2006.0008.
2. Kato JI, Hashimoto M, (2007) Construction of consecutive deletions of the Escherichia coli chromosome. Molecular Systems Biology 3: 132.
3. Christen B, Abeliuk E, Collier JM, Kalogeraki VS, Passarelli B, et al. (2011) The essential genome of a bacterium. Molecular Systems Biology 7.
4. Glass JI, Assad-Garcia N, Alperovich N, Yooseph S, Lewis MR, et al. (2006) Essential genes of a minimal bacterium. Proceedings of the National Academy of Sciences of the United States of America 103: 425-430.
5. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, et al. (2003) Essential Bacillus subtilis genes. Proceedings of the National Academy of Sciences of the United States of America 100: 4678-4683.
6. de Berardinis V, Vallenet D, Castelli V, Besnard M, Pinet A, et al. (2008) A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Molecular Systems Biology 4: 174.
7. Langridge GC, Phan MD, Turner DJ, Perkins TT, Parts L, et al. (2009) Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Research 19: 2308-2316.
8. van Opijnen T, Bodi KL, Camilli A, (2009) Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nature Methods 6: 767-U721.
9. Gallagher LA, Ramage E, Jacobst MA, Kaul R, Brittnacher M, et al. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proceedings of the National Academy of Sciences of the United States of America 104: 1009-1014.
10. French CT, Lao P, Loraine AE, Matthews BT, Yu HL, et al. (2008) Large-scale transposon mutagenesis of Mycoplasma pulmonis. Molecular Microbiology 69: 67-76.
11. Chaudhuri RR, Allen AG, Owen PJ, Shalom G, Stone K, et al. (2009) Comprehensive identification of essential Staphylococcus aureus genes using Transposon-Mediated Differential Hybridisation (TMDH). Bmc Genomics 10.
12. Jordan IK, Rogozin IB, Wolf YI, Koonin EV, (2002) Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Research 12: 962-968.
13. Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, et al. (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. Journal of Bacteriology 185: 5673-5684.
14. Rocha EPC, Danchin A, (2004) An analysis of determinants of amino acids substitution rates in bacterial proteins. Molecular Biology and Evolution 21: 108-116.
15. Silander OK, Ackermann M, (2009) The constancy of gene conservation across divergent bacterial orders. BMC Research Notes 2: 2.
16. Koonin EV, (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Reviews Microbiology 1: 127-136.
17. Geissler B, Elraheb D, Margolin W, (2003) A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 100: 4197-4202.
18. Cardinale CJ, Washburn RS, Tadigotla VR, Brown LM, Gottesman ME, et al. (2008) Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E-coli. Science 320: 935-938.
19. Alba BM, Zhong HJ, Pelayo JC, Gross CA, (2001) degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide sigma(E) activity. Molecular Microbiology 40: 1323-1333.
20. Costa CS, Pettinari MJ, Mendez BS, Anton DN, (2003) Null mutations in the essential gene yrfF (mucM) are not lethal in rcsB, yojN or rcsC strains of Salmonella enterica serovar Typhimurium. Fems Microbiology Letters 222: 25-32.
21. Peist R, Koch A, Bolek P, Sewitz S, Kolbus T, et al. (1997) Characterization of the aes gene of Escherichia coli encoding an enzyme with esterase activity. Journal of Bacteriology 179: 7679-7686.
22. Serres MH, Riley M, (2000) MultiFun, a multifunctional classification scheme for Escherichia coli K-12 gene products. Microb Comp Genomics 5: 205-222.
23. Saka K, Tadenuma M, Nakade S, Tanaka N, Sugawara H, et al. (2005) A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Research 12: 63-68.
24. Firth AE, Patrick WM, (2005) Statistics of protein library construction. Bioinformatics 21: 3314-3315.
25. Handford JI, Ize B, Buchanan G, Butland GP, Greenblatt J, et al. (2009) Conserved Network of Proteins Essential for Bacterial Viability. Journal of Bacteriology 191: 4732-4749.
26. Touati D, Jacques M, Tardat B, Bouchard L, Despied S, (1995) Lethal Oxidative Damage and Mutagenesis Are Generated by Iron in Delta-Fur Mutants of Escherichia-Coli- Protective Role of Superoxide-Dismutase. Journal of Bacteriology 177: 2305-2314.
27. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, et al. (2004) Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Molecular Microbiology 53: 1343-1357.
28. Smith TF, Waterman MS, (1981) Identification of Common Molecular Subsequences. Journal of Molecular Biology 147: 195-197.
29. Ortiz AR, Strauss CEM, Olmea O, (2002) MAMMOTH (Matching molecular models obtained from theory): An automated method for model comparison. Protein Science 11: 2606-2621.
30. Bass S, Gu QM, Christen A, (1996) Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated RlpA. Journal of Bacteriology 178: 1154-1161.
31. Barbosa JARG, Smith BJ, DeGori R, Ooi HC, Marcuccio SM, et al. (2000) Active site modulation in the N-acetylneuraminate lyase sub-family as revealed by the structure of the inhibitor-complexed Haemophilus influenzae enzyme. Journal of Molecular Biology 303: 405-421.
32. Joerger AC, Mayer S, Fersht AR, (2003) Mimicking natural evolution in vitro: An N-acetylneuraminate lyase mutant with an increased dihydrodipicolinate synthase activity. Proceedings of the National Academy of Sciences of the United States of America 100: 5694-5699.
33. Gaudu P, Weiss B, (2000) Flavodoxin mutants of Escherichia coli K-12. Journal of Bacteriology 182: 1788-1793.
34. Alba BM, Leeds JA, Onufryk C, Lu CZ, Gross CA, (2002) DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes & Development 16: 2156-2168.
35. DeLasPenas A, Connolly L, Gross CA, (1997) The sigma(E)-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigma(E). Molecular Microbiology 24: 373-385.
36. Yamanaka K, Ogura T, Koonin EV, Niki H, Hiraga S, (1994) Multicopy Suppressors, Mssa and Mssb, of an Smba Mutation of Escherichia-Coli. Molecular & General Genetics 243: 9-16.
37. Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, et al. (1991) Residual Guanosine 3′,5′-Bispyrophosphate Synthetic Activity of Rela Null Mutants Can Be Eliminated by Spot Null Mutations. Journal of Biological Chemistry 266: 5980-5990.
38. Cashel M, Gentry DR, Hernandez VJ, Vinella D, (1996) The stringent response. In: Neidhardt FC, Ingraham JL, Lin ECC, Low KB, Magasanik B, editors. Escherichia coli and Salmonella: cellular and molecular biology. 2 ed Washington D.C. American Society of Microbiology.
39. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene Ontology: tool for the unification of biology. Nature Genetics 25: 25-29.
40. Campbell TL, Ederer CS, Allali-Hassani A, Brown ED, (2007) Isolation of the rstA gene as a multicopy suppressor of YjeE, an essential ATPase of unknown function in Escherichia coli. Journal of Bacteriology 189: 3318-3321.
41. Campbell TL, Brown ED, (2008) Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. Journal of Bacteriology 190: 2537-2545.
42. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453.
43. Yu DG, Ellis HM, Lee EC, Jenkins NA, Copeland NG, et al. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 97: 5978-5983.
44. Chung CT, Niemela SL, Miller RH, (1989) One-Step Preparation of Competent Escherichia-Coli- Transformation and Storage of Bacterial-Cells in the Same Solution. Proceedings of the National Academy of Sciences of the United States of America 86: 2172-2175.
45. Miller JH, (1972) Experiments in molecular genetics New York Cold Spring Harbor Laboratory Press.
46. Cherepanov PP, Wackernagel W, (1995) Gene Disruption in Escherichia-Coli- Tcr and Km(R) Cassettes with the Option of Flp-Catalyzed Excision of the Antibiotic-Resistance Determinant. Gene 158: 9-14.
47. Bergmiller T, Pena-Miller R, Boehm A, Ackermann M, (2011) Single-cell time-lapse analysis of depletion of the universally conserved essential protein YgjD. Bmc Microbiology 11.
48. Roux A, Beloin C, Ghigo JM, (2005) Combined inactivation and expression strategy to study gene function under physiological conditions: Application to identification of new Escherichia coli adhesins. Journal of Bacteriology 187: 1001-1013.
49. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences of the United States of America 97: 6640-6645.
50. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, et al. (2005) 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 Research 12: 291-299.
51. Brickman E, Beckwith J, (1975) Analysis of Regulation of Escherichia-Coli Alkaline-Phosphatase Synthesis Using Deletions and Phi-80 Transducing Phages. Journal of Molecular Biology 96: 307-316.
52. Wall DP, Fraser HB, Hirsh AE, (2003) Detecting putative orthologs. Bioinformatics 19: 1710-1711.
53. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
54. Talavera G, Castresana J, (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564-577.
55. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
56. R Development Core Team (2007) R: A Language and Environment for Statistical Computing.
57. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R, (2006) Cyclic-di-GMP-mediated signalling within the sigma(S) network of Escherichia coli. Molecular Microbiology 62: 1014-1034.
58. Douchin V, Bohn C, Bouloc P, (2006) Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. Journal of Biological Chemistry 281: 12253-12259.
59. Cairrao F, Chora A, Zilhao R, Carpousis AJ, Arraiano CM, (2001) RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II. Molecular Microbiology 39: 1550-1561.
60. Begg KJ, Dewar SJ, Donachie WD, (1995) A New Escherichia-Coli Cell-Division Gene, Ftsk. Journal of Bacteriology 177: 6211-6222.
61. Kalamorz F, Reichenbach B, Marz W, Rak B, Gorke B, (2007) Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli. Molecular Microbiology 65: 1518-1533.
62. Draper GC, McLennan N, Begg K, Masters M, Donachie WD, (1998) Only the N-terminal domain of FtsK functions in cell division. Journal of Bacteriology 180: 4621-4627.
63. Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, et al. (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 103: 11754-11759.
64. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, et al. (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305: 1629-1631.
65. Guarino E, Jimenez-Sanchez A, Guzman EC, (2007) Defective ribonucleoside diphosphate reductase impairs replication fork progression in Escherichia coli. Journal of Bacteriology 189: 3496-3501.
66. Mileykovskaya E, Sun Q, Margolin W, Dowhan W, (1998) Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. Journal of Bacteriology 180: 4252-4257.
67. Raetz CRH, Kantor GD, Nishijima M, Newman KF, (1979) Cardiolipin Accumulation in the Inner and Outer Membranes of Escherichia-Coli Mutants Defective in Phosphatidylserine Synthetase. Journal of Bacteriology 139: 544-551.
68. Srinivasan M, Mehta P, Yu Y, Prugar E, Koonin EV, et al. (2011) The highly conserved KEOPS/EKC complex is essential for a universal tRNA modification, t6A. Embo Journal 30: 873-881.
69. Richardson JP, (1991) Preventing the Synthesis of Unused Transcripts by Rho-Factor. Cell 64: 1047-1049.
70. Hashimoto C, Sakaguchi K, Taniguchi Y, Honda H, Oshima T, et al. (2011) Effects on Transcription of Mutations in ygjD, yeaZ, and yjeE Genes, Which Are Involved in a Universal tRNA Modification in Escherichia coli. Journal of Bacteriology 193: 6075-6079.