The molecular chaperone dnak is a source of mutational robustness

Genome Biology and Evolution

Volumn 8, Issue 9, 2016, Pages 2979-2991

  Aguilar Rodríguez, José ^a,b   Sabater Muñoz, Beatriz ^c,d   Montagud Martínez, Roser ^c   Berlanga, Víctor ^c   Alvarez Ponce, David ^e   Wagner, Andreas ^a,b,f   Fares, Mario A ^c,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c Ciudad Politécnica de la Innovación   (Spain)

^d TRINITY COLLEGE DUBLIN   (Ireland)

^e UNIVERSITY OF NEVADA   (United States)

^f SANTA FE INSTITUTE   (United States)

Author keywords

Dnak; Escherichia coli; Experimental Evolution; Molecular Chaperones; Mutational Robustness; Protein Evolution

Indexed keywords

DNAK PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN 70;

ESCHERICHIA COLI; GENETICS; METABOLISM; MUTATION RATE; POINT MUTATION;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MUTATION RATE; POINT MUTATION;

EID: 84994030850     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evw176     Document Type: Article

References (59)

1. 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.
2. Barrick JE, Lenski RE. 2013. Genome dynamics during experimental evolution. Nat Rev Genet. 14:827-839.
3. Bershtein S, Mu W, Serohijos AWR, Zhou J, Shakhnovich EI. 2013. Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. Mol Cell 49:133-144.
4. Bogumil D, Dagan T. 2010. Chaperonin-dependent accelerated substitution rates in prokaryotes. Genome Biol Evol. 2:602-608.
5. Bogumil D, Dagan T. 2012. Cumulative impact of chaperone-mediated folding on genome evolution. Biochemistry 51:9941-9953.
6. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248-254.
7. Bukau B, Walker GC. 1989. Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol. 171:2337-2346.
8. Burga A, Casanueva MO, Lehner B. 2011. Predicting mutation outcome from early stochastic variation in genetic interaction partners. Nature 480:250-253.
9. Calloni G, et al. 2012. DnaK functions as a central hub in the E. Coli chaperone network. Cell Rep. 1:251-264.
10. Chen X, Zhang J. 2013. No gene-specific optimization of mutation rate in Escherichia coli. Mol Biol Evol. 30:1559-1562.
11. Cowen LE, Lindquist S. 2005. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309:2185-2189.
12. de Visser JAGM, et al. 2003. Perspective: evolution and detection of genetic robustness. Evolution 57:1959-1972.
13. Deatherage DE, Barrick JE. 2014. Identification of mutations in laboratoryevolvedmicrobes from next-generation sequencing data using breseq. Methods Mol Biol. 1151:165-188.
14. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 2005. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A. 102:14338-14343.
15. Ellis J. 1987 Proteins as molecular chaperones. Nature 328:378-379.
16. Eyre-Walker A, Keightley PD. 2007. The distribution of fitness effects of new mutations. Nat Rev Genet. 8:610-618.
17. Fares MA. 2015. The origins of mutational robustness. Trends Genet. 31:373-381.
18. Fares MA, Ruiz-González MX, Moya A, Elena SF, Barrio E. 2002. Endosymbiotic bacteria: GroEL buffers against deleterious mutations. Nature 417:398.
19. Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
20. Fujiwara K, Ishihama Y, Nakahigashi K, Soga T, Taguchi H. 2010. A systematic survey of in vivo obligate chaperonin-dependent substrates. EMBO J. 29:1552-1564.
21. Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324-332.
22. Hartl FU, Hayer-Hartl M. 2009. Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol. 16:574-581.
23. Hoffmann HJ, Lyman SK, Lu C, Petit MA, Echols H. 1992. Activity of the Hsp70 chaperone complex-DnaK, DnaJ, and GrpE-in initiating phage lambda DNA replication by sequestering and releasing lambda P protein. Proc Natl Acad Sci U S A. 89:12108-12111.
24. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:275-282.
25. Kerner MJ, et al. 2005. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122:209-220.
26. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU. 2013. Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem. 82:323-355.
27. Lachowiec J, et al. 2013. The protein chaperone HSP90 can facilitate the divergence of gene duplicates. Genetics 193:1269-1277.
28. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359.
29. Maisnier-Patin S, et al. 2005. Genomic buffering mitigates the effects of deleterious mutations in bacteria. Nat Genet. 37: 1376-1379.
30. Masel J, Siegal ML. 2009. Robustness: mechanisms and consequences. Trends Genet. 25:395-403.
31. Nishihara K, Kanemori M, Kitagawa M, Yanagi H, Yura T. 1998. Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli. Appl Environ Microbiol. 64:1694-1699.
32. Pál C, Papp B, Hurst LD. 2001. Highly expressed genes in yeast evolve slowly. Genetics 158:927-931.
33. Pechmann S, Frydman J. 2014. Interplay between chaperones and protein disorder promotes the evolution of protein networks. PLoS Comput Biol. 10:e1003674.
34. Pedersen KS, Kristensen TN, Loeschcke V. 2005. Effects of inbreeding and rate of inbreeding in Drosophilamelanogaster-Hsp70 expression and fitness. J Evol Biol. 18:756-762.
35. Powers ET, Balch WE. 2013. Diversity in the origins of proteostasis networks-A driver for protein function in evolution. Nat Rev Mol Cell Biol. 14:237-248.
36. Queitsch C, Sangster T. a, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618-624.
37. R Development Core Team. 2016. R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing.
38. Rajagopala SV, et al. 2014. The binary protein-protein interaction landscape of Escherichia coli. Nat Biotechnol. 32:285-290.
39. Rice P, Longden I, Bleasby A. 2000. EMBOSS: The european molecular biology open software suite. Trends Genet. 16:276-277.
40. Rohner N, et al. 2013. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342: 1372-1375.
41. Rudan M, Schneider D, Warnecke T, Krisko A. 2015. RNA chaperones buffer deleterious mutations in E. Coli. Elife 4:1-16.
42. Rutherford SL. 2003. Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet. 4:263-274.
43. Rutherford SL, Lindquist S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336-342.
44. Sabater-Muñoz B, et al. 2015. Fitness trade-offs determine the role of the molecular chaperonin GroEL in buffering mutations. Mol Biol Evol. 32:2681-2693.
45. Schneider C. a, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.
46. Straus D, Walter W Gross C., a 1990. DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 4:2202-2209.
47. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609-W612.
48. Tatusov RL, Koonin E, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631-637.
49. Tokuriki N, Stricher F, Serrano L, Tawfik DS. 2008. How protein stability and new functions trade off. PLoS Comput Biol. 4:e1000002.
50. Tokuriki N, Tawfik DS. 2009. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459:668-673.
51. Turrientes M-C, et al. 2013. Normal mutation rate variants arise in a mutator (Mut S) Escherichia coli population. PLoS One 8:e72963.
52. Wagner A. 2005. Robustness and evolvability in living systems. Princeton (NJ): Princeton University Press.
53. Warnecke T. 2012. Loss of the DnaK-DnaJ-GrpE chaperone system among the Aquificales. Mol Biol Evol. 29:3485-3495.
54. Warnecke T, Hurst LD. 2010. GroEL dependency affects codon usage-support for a critical role of misfolding in gene evolution. Mol Syst Biol. 6:340.
55. Williams TA, Fares MA. 2010. The effect of chaperonin buffering on protein evolution. Genome Biol Evol. 2:609-619.
56. Wyganowski KT, Kaltenbach M, Tokuriki N. 2013. GroEL/ES buffering and compensatory mutations promote protein evolution by stabilizing folding intermediates. J Mol Biol. 425:3403-3414.
57. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
58. Young JC, Agashe VR, Siegers K, Hartl FU. 2004. Pathways of chaperonemediated protein folding in the cytosol. Nat Rev Mol Cell Biol. 5:781-791.
59. Zhang J, Yang J-R. 2015. Determinants of the rate of protein sequence evolution. Nat Rev Genet. 16:409-420.