Genome instability mediates the loss of key traits by Acinetobacter baylyi ADP1 during laboratory evolution

Journal of Bacteriology

Volumn 197, Issue 5, 2015, Pages 872-881

  Renda, Brian A ^a   Dasgupta, Aurko ^a   Leon, Dacia ^a   Barrick, Jeffrey E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACINETOBACTER BAYLYI; ACINETOBACTER BAYLYI ADP1; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MUTATION; BROTH DILUTION; CELL AGGREGATION; CONTROLLED STUDY; DNA INTEGRATION; GENE DELETION; GENE LOSS; GENETIC TRAIT; GENOMIC INSTABILITY; LABORATORY; METABOLIC ENGINEERING; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROPHAGE; REPRODUCTIVE FITNESS; SEQUENCE ANALYSIS; TRANSPOSON; WHOLE GENOME SEQUENCING; ACINETOBACTER; BACTERIUM TRANSFORMATION; GENETICS;

ACINETOBACTER BAYLYI; BACTERIA (MICROORGANISMS);

BACTERIAL PROTEIN; TRANSPOSON;

ACINETOBACTER; BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; GENOMIC INSTABILITY; METABOLIC ENGINEERING; PHENOTYPE; SEQUENCE DELETION; TRANSFORMATION, BACTERIAL;

EID: 84961287763     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02263-14     Document Type: Article

References (53)

1. Esvelt KM, Wang HH. 2013. Genome-scale engineering for systems and synthetic biology. Mol Syst Biol 9:641. http://dx.doi.org/10.1038/msb .2012.66.
2. Pál C, Papp B, Pósfai G. 2014. The dawn of evolutionary genome engineering. Nat Rev Genet 15:504-512. http://dx.doi.org/10.1038/nrg3746.
3. Pósfai G, Plunkett G, Fehér T, Frisch D, Keil GM, Umenhoffer K, Kolisnychenko V, Stahl B, Sharma SS, de Arruda M, Burland V, Harcum SW, Blattner FR. 2006. Emergent properties of reduced-genome Escherichia coli. Science 312:1044-1046. http://dx.doi.org/10.1126 /science.1126439.
4. Lajoie MJ, Rovner AJ, Goodman DB, Aerni H-R, Haimovich AD, Kuznetsov G, Mercer JA, Wang HH, Carr PA, Mosberg JA, Rohland N, Schultz PG, Jacobson JM, Rinehart J, Church GM, Isaacs FJ. 2013. Genomically recoded organisms expand biological functions. Science 342: 357-360. http://dx.doi.org/10.1126/science.1241459.
5. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM. 2009. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:894 -898. http://dx.doi.org/10.1038 /nature08187.
6. De Berardinis V, Durot M, Weissenbach J, Salanoubat M. 2009. Acinetobacter baylyi ADP1 as a model for metabolic system biology. Curr Opin Microbiol 12:568-576. http://dx.doi.org/10.1016/j.mib.2009.07.005.
7. Elliott KT, Neidle EL. 2011. Acinetobacter baylyi ADP1: transforming the choice of model organism. IUBMB Life 63:1075-1080. http://dx.doi.org /10.1002/iub.530.
8. Metzgar D, Bacher JM, Pezo V, Reader J, Döring V, Schimmel P, Marlière P, de Crécy-Lagard V. 2004. Acinetobacter sp. ADP1: an ideal model organism for genetic analysis and genome engineering. Nucleic Acids Res 32:5780-5790. http://dx.doi.org/10.1093/nar/gkh881.
9. Palmen R, Vosman B, Buijsman P, Breek CKD, Hellingwerf KJ. 1993. Physiological characterization of natural transformation in Acinetobacter calcoaceticus. J Gen Microbiol 139:295-305. http://dx.doi.org/10.1099 /00221287-139-2-295.
10. Simpson D, Dawson L, Fry J. 2007. Influence of flanking homology and insert size on the transformation frequency of Acinetobacter baylyi BD413. Environ Biosafety Res 6:55-69. http://dx.doi.org/10.1051/ebr:2007027.
11. Datsenko K, Wanner B. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
12. Bacher JM, Metzgar D, de Crécy-Lagard V. 2006. Rapid evolution of diminished transformability in Acinetobacter baylyi. J Bacteriol 188:8534-8542. http://dx.doi.org/10.1128/JB.00846-06.
13. Umenhoffer K, Fehér T, Balikó G, Ayaydin F, Pósfai J, Blattner FR, Pósfai G. 2010. Reduced evolvability of Escherichia coli MDS42, an IS-less cellular chassis for molecular and synthetic biology applications. Microb Cell Fact 9:38. http://dx.doi.org/10.1186/1475-2859-9-38.
14. Darmon E, Leach DRF. 2014. Bacterial genome instability. Microbiol Mol Biol Rev 78:1-39. http://dx.doi.org/10.1128/MMBR.00035-13.
15. De Berardinis V, Vallenet D, Castelli V, Besnard M, Pinet A, Cruaud C, Samair S, Lechaplais C, Gyapay G, Richez C, Durot M, Kreimeyer A, Le Fèvre F, Schächter V, Pezo V, Döring V, Scarpelli C, Médigue C, Cohen GN, Marlière P, Salanoubat M, Weissenbach J. 2008. A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Mol Syst Biol 4:174. http://dx.doi.org/10.1038/msb.2008.10.
16. Dong D, Yan A, Liu H, Zhang X, Xu Y. 2006. Removal of humic substances from soil DNA using aluminium sulfate. J Microbiol Methods 66:217-222. http://dx.doi.org/10.1016/j.mimet.2005.11.010.
17. Murin CD, Segal K, Bryksin A, Matsumura I. 2012. Expression vectors for the engineering of genes and genomes in Acinetobacter baylyi ADP1. Appl Environ Microbiol 78:280-283. http://dx.doi.org/10.1128 /AEM.05597-11.
18. Woods RJ, Barrick JE, Cooper TF, Shrestha U, Kauth MR, Lenski RE. 2011. Second-order selection for evolvability in a large Escherichia coli population. Science 331:1433-1436. http://dx.doi.org/10.1126/science .1198914.
19. Baker GC, Smith JJ, Cowan DA. 2003. Review and re-analysis of domainspecific 16S primers. J Microbiol Methods 55:541-555. http://dx.doi.org /10.1016/j.mimet.2003.08.009.
20. Barbe V, Vallenet D, Fonknechten N, Kreimeyer A, Oztas S, Labarre L, Cruveiller S, Robert C, Duprat S, Wincker P, Ornston LN, Weissenbach J, Marlière P, Cohen GN, Médigue C. 2004. Unique features revealed by the genome sequence of Acinetobacter sp. ADP1, a versatile and naturally transformation competent bacterium. Nucleic Acids Res 32:5766-5779. http://dx.doi.org/10.1093/nar/gkh910.
21. Deatherage DE, Barrick JE. 2014. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 1151:165-188. http://dx.doi.org/10.1007/978-1 -4939-0554-6_12.
22. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi .org/10.1101/gr.074492.107.
23. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402. http: //dx.doi.org/10.1093/nar/25.17.3389.
24. R Development Core Team. 2014. R: a language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria.
25. Toren A, Navon-Venezia S, Ron EZ, Rosenberg E. 2001. Emulsifying activities of purified alasan proteins from Acinetobacter radioresistens KA53. Appl Environ Microbiol 67:1102-1106. http://dx.doi.org/10.1128 /AEM.67.3.1102-1106.2001.
26. Kibota TT, Lynch M. 1996. Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381:694-696. http://dx.doi.org /10.1038/381694a0.
27. Barrick JE, Lenski RE. 2013. Genome dynamics during experimental evolution. Nat Rev Genet 14:827-839. http://dx.doi.org/10.1038/nrg3564.
28. Zolkiewski M. 2006. A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol 61:1094-1100. http: //dx.doi.org/10.1111/j.1365-2958.2006.05309.x.
29. Gottesman S, Clark WP, Maurizi MR. 1990. The ATP-dependent Clp protease of Escherichia coli. Sequence of clpA and identification of a Clpspecific substrate. J Biol Chem 265:7886-7893.
30. Segura A, Bünz PV, D'Argenio DA, Ornston LN. 1999. Genetic analysis of a chromosomal region containing vanA and vanB, genes required for conversion of either ferulate or vanillate to protocatechuate in Acinetobacter. J Bacteriol 181:3494-3504.
31. Averhoff B, Graf I. 2008. The natural transformation system of Acinetobacter baylyi ADP1: a unique dna transport machinery, p 119-139. In Gerischer U (ed), Acinetobacter molecular biology. Caister Academic Press, Norfolk, United Kingdom.
32. Link C, Eickernjäger S, Porstendörfer D, Averhoff B. 1998. Identification and characterization of a novel competence gene, comC, required for DNA binding and uptake in Acinetobacter sp. strain BD413. J Bacteriol 180:1592-1595.
33. Nakar D, Gutnick DL. 2001. Analysis of the wee gene cluster responsible for the biosynthesis of the polymeric bioemulsifier from the oil-degrading strain Acinetobacter lwoffii RAG-1. Microbiology 147:1937-1946.
34. Vaneechoutte M, Tjernberg I, Baldi F, Pepi M, Fani R. 1999. Oil-degrading Acinetobacter strain RAG-1 and strains described as "Acinetobacter venetianus sp. nov." belong to the same genomic species. Res Microbiol 150: 69-73. http://dx.doi.org/10.1016/S0923-2508(99)80047-3.
35. Kaplan N, Rosenberg E. 1982. Exopolysaccharide distribution of and bioemulsifier production by Acinetobacter calcoaceticus BD4 and BD413. Appl Environ Microbiol 44:1335-1341.
36. Kaplan N, Zosim Z, Rosenberg E. 1987. Reconstitution of emulsifying activity of Acinetobacter calcoaceticus BD4 emulsan by using pure polysaccharide and protein. Appl Environ Microbiol 53:440-446.
37. Gerischer U, Argenio DAD, Ornston LN. 1996. IS1236, a newly discovered member of the IS3 family, exhibits varied patterns of insertion into the Acinetobacter calcoaceticus chromosome. Microbiology 142:1825-1831. http://dx.doi.org/10.1099/13500872-142-7-1825.
38. Duval-Valentin G, Marty-Cointin B, Chandler M. 2004. Requirement of IS911 replication before integration defines a new bacterial transposition pathway. EMBO J 23:3897-3906. http://dx.doi.org/10 .1038/sj.emboj.7600395.
39. Cuff LE, Elliott KT, Seaton SC, Ishaq MK, Laniohan NS, Karls AC, Neidle EL. 2012. Analysis of IS1236-mediated gene amplification events in Acinetobacter baylyi ADP1. J Bacteriol 194:4395-4405. http://dx.doi .org/10.1128/JB.00783-12.
40. Jezequel N, Lagomarsino MC, Heslot F, Thomen P. 2013. Long-term diversity and genome adaptation of Acinetobacter baylyi in a minimalmedium chemostat. Genome Biol Evol 5:87-97. http://dx.doi.org/10.1093 /gbe/evs120.
41. Welty DJ, Jones JM, Nakai H. 1997. Communication of ClpXP protease hypersensitivity to bacteriophage Mu repressor isoforms. J Mol Biol 272: 31-41. http://dx.doi.org/10.1006/jmbi.1997.1193.
42. Sekine Y, Izumi K, Mizuno T, Ohtsubo E. 1997. Inhibition of transpositional recombination by OrfA and OrfB proteins encoded by insertion sequence IS3. Genes Cells 2:547-557.
43. Tenaillon O, Taddei F, Radmian M, Matic I. 2001. Second-order selection in bacterial evolution: selection acting on mutation and recombination rates in the course of adaptation. Res Microbiol 152:11-16. http://dx .doi.org/10.1016/S0923-2508(00)01163-3.
44. Philippe N, Crozat E, Lenski RE, Schneider D. 2007. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29:846-860. http://dx.doi.org/10.1002/bies.20629.
45. Conrad TM, Lewis NE, Palsson BO. 2011. Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol 7:509. http://dx.doi .org/10.1038/msb.2011.42.
46. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461:1243-1247. http://dx.doi.org/10 .1038/nature08480.
47. Palmen R, Hellingwerf KJ. 1995. Acinetobacter calcoaceticus liberates chromosomal DNA during induction of competence by cell lysis. Curr Microbiol 30:7-10. http://dx.doi.org/10.1007/BF00294516.
48. Vaneechoutte M, Young DM, Ornston LN, De Baere T, Nemec A, Van Der Reijden T, Carr E, Tjernberg I, Dijkshoorn L. 2006. Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi. Appl Environ Microbiol 72:932. http: //dx.doi.org/10.1128/AEM.72.1.932-936.2006.
49. Juni E, Janik A. 1969. Transformation of Acinetobacter calco-aceticus (Bacterium anitratum). J Bacteriol 98:281-288.
50. Williams KP. 2002. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30:866-875. http://dx.doi.org/10.1093/nar/30.4.866.
51. Cooper VS, Schneider D, Blot M, Lenski RE. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183:2834-2841. http://dx.doi.org/10.1128 /JB.183.9.2834-2841.2001.
52. Dalia AB, McDonough E, Camilli A. 2014. Multiplex genome editing by natural transformation. Proc Natl Acad Sci U S A 111:8937-8942. http: //dx.doi.org/10.1073/pnas.1406478111.
53. Renda BA, Hammerling MJ, Barrick JE. 2014. Engineering reduced evolutionary potential for synthetic biology. Mol Biosyst 10:1668-1678. http://dx.doi.org/10.1039/c3mb70606k.