Assessing the benefits of horizontal gene transfer by laboratory evolution and genome sequencing

BMC Evolutionary Biology

Volumn 18, Issue 1, 2018, Pages

  Chu, Hoi Yee ^a   Sprouffske, Kathleen ^b   Wagner, Andreas ^a,b,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c SANTA FE INSTITUTE   (United States)

Author keywords

Experimental evolution; Horizontal gene transfer; Novel nutrient adaptation

Indexed keywords

ADAPTATION; ASSESSMENT METHOD; BACTERIUM; CHEMICAL COMPOUND; COLIFORM BACTERIUM; DNA; EVOLUTION; FITNESS; GENE TRANSFER; GENOME; LABORATORY METHOD; MUTATION; PROKARYOTE; RECOMBINATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA;

4-HYDROXYPHENYLACETIC ACID; BUTYRIC ACID; PHENYLACETIC ACID DERIVATIVE;

ADAPTATION; BACTERIAL GENOME; DIRECTED MOLECULAR EVOLUTION; DNA SEQUENCE; ESCHERICHIA COLI; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; MOLECULAR EVOLUTION; MUTATION; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PHENOTYPE;

ADAPTATION, PHYSIOLOGICAL; BASE SEQUENCE; BUTYRIC ACID; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; MUTATION; OPEN READING FRAMES; OPERON; PHENOTYPE; PHENYLACETATES; SEQUENCE ANALYSIS, DNA;

EID: 85045632836     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-018-1164-7     Document Type: Article

References (104)

1. Wozniak RAF, Waldor MK. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol. 2010;8:552-63.
2. Lang AS, Zhaxybayeva O, Beatty JT. Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol. 2012;10:472-82.
3. Johnston C, Martin B, Fichant G, Polard P, Claverys J-P. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol. 2014;12:181-96.
4. Andam CP, Gogarten JP. Biased gene transfer in microbial evolution. Nat Rev Microbiol. 2011;9:543-55.
5. Thompson JR. Genotypic diversity within a natural coastal Bacterioplankton population. Sci. 2005;307:1311-3. doi:10.1126/science.1106028
6. Vos M, Hesselman MC, te Beek TA, van Passel MWJ, Eyre-Walker A. Rates of lateral gene transfer in prokaryotes: high but why? Trends Microbiol. 2015;23:598-605.
7. Koonin E V. Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Research. 2016;5. https://doi.org/10.12688/f1000research.8737.1.
8. Thomas CM, Nielsen KM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol. 2005;3:711-21.
9. Mazel D. Integrons: agents of bacterial evolution. Nat Rev Micro. 2006;4:608-20. https://doi.org/10.1038/nrmicro1462
10. Ram Y, Hadany L. Condition-dependent sex: who does it, when and why? Phil Trans R Soc B. 2016;371:20150539.
11. Hanage WP. Not so simple after all: Bacteria, their population genetics, and recombination. Cold Spring Harb Perspect Biol. 2016;:a018069. https://doi.org/10.1101/cshperspect.a018069.
12. Treangen TJ, Rocha EPC. Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet. 2011;7:e1001284.
13. Croucher NJ, Mostowy R, Wymant C, Turner P, Bentley SD, Fraser C. Horizontal DNA transfer mechanisms of bacteria as weapons of intragenomic conflict. PLoS Biol. 2016;14:e1002394.
14. Touchon M, Bobay L-M, Rocha EPC. The chromosomal accommodation and domestication of mobile genetic elements. Curr Opin Microbiol. 2014;22:22-9.
15. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev. 2009;33:376-93.
16. Dillingham MS, Kowalczykowski SC. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol Mol Biol Rev. 2008;72:642-71. https://doi.org/10.1128/MMBR.00020-08.
17. Rocha EPC, Cornet E, Michel B. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet. 2005;1:e15.
18. Hoelzer MA, Michod RE. DNA repair and the evolution of transformation in Bacillus subtilis. III. Sex with damaged DNA. Genetics. 1991;128:215-23.
19. López-Pérez M, Martin-Cuadrado AB, Rodriguez-Valera F. Homologous recombination is involved in the diversity of replacement flexible genomic islands in aquatic prokaryotes. Front Genet. 2014;5:147.
20. Milkman R, Bridges MM. Molecular evolution of the Escherichia Coli chromosome. III. Clonal frames. Genetics. 1990;126:505-17.
21. Guttman DS, Dykhuizen DE. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science. 1994;266:1380.
22. Didelot X, Meric G, Falush D, Darling AE. Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genomics. 2012;13:256.
23. Rodriguez-Valera F, Martin-Cuadrado AB, López-Pérez M. Flexible genomic islands as drivers of genome evolution. Curr Opin Microbiol. 2016;31:154-60.
24. Land M, Hauser L, Jun S-R, Nookaew I, Leuze MR, Ahn T-H, et al. Insights from 20 years of bacterial genome sequencing. Funct Integr Genomics. 2015;15:141-61. https://doi.org/10.1007/s10142-015-0433-4.
25. Lapierre P, Gogarten JP. Estimating the size of the bacterial pan-genome. Trends Genet. 2009;25:107-10.
26. Park C, Zhang J. High expression hampers horizontal gene transfer. Genome Biol Evol. 2012;4:523-32.
27. Deem MW. Statistical mechanics of modularity and horizontal gene transfer. Annu Rev Condens Matter Phys. 2013;4:287-311.
28. Hall JPJ, Brockhurst MA, Harrison E. Sampling the mobile gene pool: innovation via horizontal gene transfer in bacteria. Philos Trans R Soc B Biol Sci. 2017;372:20160424. https://doi.org/10.1098/rstb.2016.0424.
29. Lukjancenko O, Wassenaar TM, Ussery DW. Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol. 2010;60:708-20.
30. Hehemann J-H, Arevalo P, Datta MS, Yu X, Corzett CH, Henschel A, et al. Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes. Nat Commun. 2016;7:12860.
31. Hemme CL, Green SJ, Rishishwar L, Prakash O, Pettenato A, Chakraborty R, et al. Lateral gene transfer in a heavy metal-contaminated-groundwater microbial community. MBio. 2016;7:e02234-15.
32. Zhang X, Liu X, Liang Y, Guo X, Xiao Y, Ma L, et al. Adaptive evolution of extreme acidophile Sulfobacillus thermosulfidooxidans potentially driven by horizontal gene transfer and gene loss. Appl Environ Microbiol. 2017;83:03098.
33. Broaders E, O'Brien C, Gahan CGM, Marchesi JR. Evidence for plasmid-mediated salt tolerance in the human gut microbiome and potential mechanisms. FEMS Microbiol Ecol. 2016;92:fiw019.
34. Brito IL, Yilmaz S, Huang K, Xu L, Jupiter SD, Jenkins AP, et al. Mobile genes in the human microbiome are structured from global to individual scales. Nature. 2016;535:435.
35. Pang TY, Lercher M. The adaptive acquisition of single DNA segments drives metabolic evolution across E. coli lineages. bioRxiv. 2017. doi: https://doi.org/10.1101/148460.
36. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLoS Comput Biol. 2015;11:e1004095.
37. Lu B, Leong HW. Computational methods for predicting genomic islands in microbial genomes. Comput Struct Biotechnol J. 2016;14:200-6.
38. Boritsch EC, Khanna V, Pawlik A, Honoré N, Navas VH, Ma L, et al. Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria. Proc Natl Acad Sci. 2016;113:9876-81.
39. McCarthy AJ, Loeffler A, Witney AA, Gould KA, Lloyd DH, Lindsay JA. Extensive horizontal gene transfer during Staphylococcus aureus co-colonization in vivo. Genome Biol Evol. 2014;6:2697-708.
40. Baltrus DA. Exploring the costs of horizontal gene transfer. Trends Ecol Evol. 2013;28:489-95.
41. Bailey SF, Bataillon T. Can the experimental evolution programme help us elucidate the genetic basis of adaptation in nature? Mol Ecol. 2016;25:203-18.
42. Giraud T, Koskella B, Laine A. Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution. Mol Ecol. 2017;26:1703-10.
43. Souza V, Turner PE, Lenski RE. Long-term experimental evolution in Escherichia coli. V. Effects of recombination with immigrant genotypes on the rate of bacterial evolution. J Evol Biol. 1997;10:743-69.
44. Lind PA, Tobin C, Berg OG, Kurland CG, Andersson DI. Compensatory gene amplification restores fitness after inter-species gene replacements. Mol Microbiol. 2010;75:1078-89.
45. Knöppel A, Lind PA, Lustig U, Näsvall J, Andersson DI. Minor fitness costs in an experimental model of horizontal gene transfer in bacteria. Mol Biol Evol. 2014;31:1220. msu076
46. Dougherty K, Smith BA, Moore AF, Maitland S, Fanger C, Murillo R, et al. Multiple phenotypic changes associated with large-scale horizontal gene transfer. PLoS One. 2014;9:e102170.
47. San Millan A, Toll-Riera M, Qi Q, MacLean RC. Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa. Nat Commun. 2015;6:6845.
48. San Millan A, Escudero JA, Gifford DR, Mazel D, MacLean RC. Multicopy plasmids potentiate the evolution of antibiotic resistance in bacteria. Nat Ecol Evol. 2016;1:10.
49. Bedhomme S, Perez Pantoja D, Bravo IG. Plasmid and clonal interference during post horizontal gene transfer evolution. Mol Ecol. 2017;26:1832-47.
50. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000;405:299-304.
51. Archer CT, Kim JF, Jeong H, Park JH, Vickers CE, Lee SY, et al. The genome sequence of E. Coli W (ATCC 9637): comparative genome analysis and an improved genome-scale reconstruction of E. Coli. BMC Genomics. 2011;12:1.
52. Baumler DJ, Peplinski RG, Reed JL, Glasner JD, Perna NT. The evolution of metabolic networks of E. Coli. BMC Syst Biol. 2011;5:1.
53. Yoon SH, Han M-J, Jeong H, Lee CH, Xia X-X, Lee D-H, et al. Comparative multi-omics systems analysis of Escherichia coli strains B and K-12. Genome Biol. 2012;13:1.
54. Monk JM, Charusanti P, Aziz RK, Lerman JA, Premyodhin N, Orth JD, et al. Genome-scale metabolic reconstructions of multiple Escherichia coli strains highlight strain-specific adaptations to nutritional environments. Proc Natl Acad Sci. 2013;110:20338-43.
55. Prieto AA, Di E. Molecular characterization of the 4-Hydroxyphenylacetate catabolic pathway of. Microbiology. 1996;178:111-20.
56. Fuchs G, Boll M, Heider J. Microbial degradation of aromatic compounds - from one strategy to four. Nat Rev Microbiol. 2011;9:803-16.
57. Shrivastava R, Purohit H, Phale PS. Metabolism and preferential utilization of phenylacetic acid and 4-hydroxyphenylacetic acid in Pseudomonas putida CSV86. J Bioremed Biodegrad. 2011;2:120.
58. Klein K, Steinberg R, Fiethen B, Overath P. Fatty acid degradation in Escherichia coli. Eur J Biochem. 1971;19:442-50.
59. Iram SH, Cronan JE. The β-oxidation systems of Escherichia coli and Salmonella enterica are not functionally equivalent. J Bacteriol. 2006;188:599-608.
60. Jenkins LS, Nunn WD. Genetic and molecular characterization of the genes involved in short-chain fatty acid degradation in Escherichia coli: the ato system. J Bacteriol. 1987;169:42-52.
61. Pauli G, Overath P. Ato operon: a highly inducible system for acetoacetate and butyrate degradation in Escherichia coli. Eur J Biochem. 1972;29:553-62.
62. Liu X, Zhu Y, Yang S. Construction and characterization of ack deleted mutant of Clostridium tyrobutyricum for enhanced butyric acid and hydrogen production. Biotechnol Prog. 2006;22:1265-75.
63. Barth E, Gora KV, Gebendorfer KM, Settele F, Jakob U, Winter J. Interplay of cellular cAMP levels, s S activity and oxidative stress resistance in Escherichia coli. Microbiology. 2009;33:1680-9.
64. Winkler J, Kao KC. Harnessing recombination to speed adaptive evolution in Escherichia coli. Metab Eng. 2012;14:487-95.
65. Jeong H, Barbe V, Lee CH, Vallenet D, Yu DS, Choi S-H, et al. Genome sequences of Escherichia coli B strains REL606 and BL21 (DE3). J Mol Biol. 2009;394:644-52.
66. Cooper TF, Rozen DE, Lenski RE. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci. 2003;100:1072-7.
67. Dragosits M, Mozhayskiy V, Quinones-Soto S, Park J, Tagkopoulos I. Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli. Mol Syst Biol. 2013;9:643.
68. Garst AD, Bassalo MC, Pines G, Lynch SA, Halweg-Edwards AL, Liu R, et al. Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering. Nat Biotechnol. 2016;35:48.
69. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, et al. The molecular diversity of adaptive convergence. Science. 2012;335:457-61.
70. Li M, Ho PY, Yao S, Shimizu K. Effect of sucA or sucC gene knockout on the metabolism in Escherichia coli based on gene expressions, enzyme activities, intracellular metabolite concentrations and metabolic fluxes by 13 C-labeling experiments. Biochem Eng J. 2006;30:286-96.
71. Phue J-N, Lee SJ, Kaufman JB, Negrete A, Shiloach J. Acetate accumulation through alternative metabolic pathways in ackA- pta- poxB- triple mutant in E. Coli B (BL21). Biotechnol Lett. 2010;32:1897-903.
72. Zawadzki P, Roberts MS, Cohan FM. The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics. 1995;140:917-32.
73. Hüttener M, Paytubi S, Juárez A. Success in incorporating horizontally transferred genes: the H-NS protein. Trends Microbiol. 2015;23:67-9.
74. Brass EP. Overview of coenzyme a metabolism and its role in cellular toxicity. Chem Biol Interact. 1994;90:203-14.
75. Lennen RM, Kruziki MA, Kumar K, Zinkel RA, Burnum KE, Lipton MS, et al. Membrane stresses induced by overproduction of free fatty acids in Escherichia coli. Appl Environ Microbiol. 2011;77:8114-28.
76. López-Villamizar I, Cabezas A, Pinto RM, Canales J, Ribeiro JM, Cameselle JC, et al. The characterization of Escherichia coli CpdB as a recombinant protein reveals that, besides having the expected 3-Nucleotidase and 2′, 3-cyclic mononucleotide phosphodiesterase activities, it is also active as cyclic dinucleotide phosphodiesterase. PLoS One. 2016;11:e0157308.
77. Imamura R, Yamanaka K, Ogura T, Hiraga S, Fujita N, Ishihama A, et al. Identification of the cpdA gene encoding cyclic 3′, 5′-adenosine monophosphate phosphodiesterase in Escherichia coli. J Biol Chem. 1996;271:25423-9.
78. Battesti A, Majdalani N, Gottesman S. The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol. 2011;65:189-213.
79. Basak S, Jiang R. Enhancing E. Coli tolerance towards oxidative stress via engineering its global regulator cAMP receptor protein (CRP). PLoS One. 2012;7:e51179.
80. Bren A, Park JO, Towbin BD, Dekel E, Rabinowitz JD, Alon U. Glucose becomes one of the worst carbon sources for E. Coli on poor nitrogen sources due to suboptimal levels of cAMP. Sci Rep. 2016;6:24834.
81. Feng Y, Cronan JE. Crosstalk of Escherichia coli FadR with global regulators in expression of fatty acid transport genes. PLoS One. 2012;7:e46275.
82. Nam H, Lewis NE, Lerman JA, Lee D-H, Chang RL, Kim D, et al. Network context and selection in the evolution to enzyme specificity. Science. 2012;337:1101. LP - 1104
83. Notebaart RA, Szappanos B, Kintses B, Pál F, Györkei Á, Bogos B, et al. Network-level architecture and the evolutionary potential of underground metabolism. Proc Natl Acad Sci. 2014;111:11762-7.
84. Rosen MJ, Davison M, Bhaya D, Fisher DS. Fine-scale diversity and extensive recombination in a quasisexual bacterial population occupying a broad niche. Science. 2015;348:1019-23.
85. Culligan EP, Sleator RD, Marchesi JR, Hill C. Metagenomic identification of a novel salt tolerance gene from the human gut microbiome which encodes a membrane protein with homology to a brp/blh-family β-carotene 15, 15′-monooxygenase. PLoS One. 2014;9:e103318.
86. Thies S, Rausch SC, Kovacic F, Schmidt-Thaler A, Wilhelm S, Rosenau F, et al. Metagenomic discovery of novel enzymes and biosurfactants in a slaughterhouse biofilm microbial community. Sci Rep. 2016;6:27035.
87. Studier FW, Daegelen P, Lenski RE, Maslov S, Kim JF. Understanding the differences between genome sequences of Escherichia coli B strains REL606 and BL21 (DE3) and comparison of the E. Coli B and K-12 genomes. J Mol Biol. 2009;394:653-80.
88. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006;2. https://doi.org/10.1038/msb4100050.
89. Achtman M, Kennedy N, Skurray R. Cell - cell interactions in conjugating Escherichia coli: role of traT protein in surface exclusion. Proc Natl Acad Sci. 1977;74:5104-8.
90. Orth JD, Thiele I, Palsson BØ. What is flux balance analysis? Nat Biotechnol. 2010;28:245-8.
91. Gamo M, Shoji T. A method of profiling microbial communities based on a most-probable-number assay that uses BIOLOG plates and multiple sole carbon sources. Appl Environ Microbiol. 1999;65:4419-24.
92. Leiby N, Marx CJ. Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biol. 2014;12:e1001789.
93. Jenkins LS, Nunn WD. Regulation of the ato operon by the atoC gene in Escherichia coli. J Bacteriol. 1987;169:2096-102.
94. Sprouffske K, Wagner A. Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinformatics. 2016;17:172.
95. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297-303.
96. Dixit PD, Pang TY, Studier FW, Maslov S. Recombinant transfer in the basic genome of {E}scherichia coli. Proc Natl Acad Sci. 2015;112:9070-5.
97. Langmead B, Salzberg SL. Fast gapped-read alignment with {B}owtie 2. Nat Methods. 2012;9:357-9.
98. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly (Austin). 2012;6:80-92. https://doi.org/10.4161/fly.19695.
99. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614. gkw569
100. Darling AE, Mau B, Perna NT. Progressive Mauve: Multiple alignment of genomes with gene flux and rearrangement. Genome. 2009. http://arxiv.org/abs/0910.5780.
101. Yoon S-H, Ha S, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek. 2017;110:1281-6. https://doi.org/10.1007/s10482-017-0844-4.
102. R Core Team. R: A Language and Environment for Statistical Computing. 2015. http://www.r-project.org /.
103. Dhar R, Sägesser R, Weikert C, Wagner A. Yeast adapts to a changing stressful environment by evolving cross-protection and anticipatory gene regulation. Mol Biol Evol. 2013;30:573-88.
104. Hothorn T, Hornik K, Hothorn MT. Package "exactRankTests." 2015. https://CRAN.R-project.org/package=exactRankTests. Accessed 1 Mar 2017.