Genome-wide identification of tolerance mechanisms toward p-coumaric acid in Pseudomonas putida

Biotechnology and Bioengineering

Volumn 115, Issue 3, 2018, Pages 762-774

  Calero, Patricia ^a   Jensen, Sheila I ^a   Bojanovič, Klara ^a   Lennen, Rebecca M ^a   Koza, Anna ^a   Nielsen, Alex T ^a  

^a Technical University of Denmark   (Denmark)

Author keywords

p coumaric acid; Pseudomonas putida; Tn seq; tolerance

Indexed keywords

ESCHERICHIA COLI; FITS AND TOLERANCES;

CYTOCHROME C MATURATION SYSTEMS; HIGH-THROUGHPUT SEQUENCING; MEMBRANE INTEGRITY; MEMBRANE STABILITY; P-COUMARIC ACID; PSEUDOMONAS PUTIDA; TN-SEQ; TOLERANCE MECHANISMS;

GENES;

PARA COUMARIC ACID; PROPIONIC ACID DERIVATIVE; TRANS-3-(4'-HYDROXYPHENYL)-2-PROPENOIC ACID;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; CYTOCHROME C MATURATION GENE; ESCHERICHIA COLI; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; NONHUMAN; PSEUDOMONAS PUTIDA; TTG2ABC GENE; ANTIBIOTIC RESISTANCE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM;

DRUG RESISTANCE, BACTERIAL; GENOME-WIDE ASSOCIATION STUDY; PROPIONATES; PSEUDOMONAS PUTIDA;

EID: 85036507453     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.26495     Document Type: Article

References (76)

1. Abril, M. A., Michan, C., Timmis, K. N., & Ramos, J. L. (1989). Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway. Journal of Bacteriology, 171, 6782–6790.
2. Alper, H., Moxley, J., Nevoigt, E., Fink, G. R., & Stephanopoulos, G. (2006). Tolerance and Production. Science, 314, 1565–1568.
3. Atsumi, S., Wu, T.-Y., Machado, I. M. P., Huang, W.-C., Chen, P.-Y., Pellegrini, M., & Liao, J. C. (2010). Evolution, genomic analysis, and reconstruction of isobutanol tolerance in Escherichia coli. Molecular Systems Biology, 6, 449. https://doi.org/10.1038/msb.2010.98
4. Baert, B., Baysse, C., Matthijs, S., & Cornelis, P. (2008). Multiple phenotypic alterations caused by a c-type cytochrome maturation ccmC gene mutation in Pseudomonas aeruginosa. Microbiology, 154, 127–138.
5. Bagdasarian, M., Lurz, R., Rückert, B., Franklin, F. C. H., Bagdasarian, M. M., Frey, J., & Timmis, K. N. (1981). Specific-purpose plasmid cloning vectors II. Broad host range, high copy number, RSF 1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. Gene, 16, 237–247.
6. Barquist, L., Boinett, C. J., & Cain, A. K. (2013). Approaches to querying bacterial genomes with transposon-insertion sequencing. RNA Biology, 10, 1161–1169.
7. Benndorf, D., Thiersch, M., Loffhagen, N., Kunath, C., & Harms, H. (2006). Pseudomonas putida KT2440 responds specifically to chlorophenoxy herbicides and their initial metabolites. Proteomics, 6, 3319–3329.
8. Calero, P., Jensen, S. I., & Nielsen, A. T. (2016). Broad-Host-Range ProUSER vectors enable fast characterization of inducible promoters and optimization of p-Coumaric acid production in Pseudomonas putida KT2440. ACS Synthetic Biology, 5, 741–753.
9. Carpenter, C. D., Cooley, B. J., Needham, B. D., Fisher, C. R., Trent, M. S., Gordon, V., & Paynea, S. M. (2014). The Vps/VacJ ABC transporter is required for intercellular spread of Shigella flexneri. Infection and Immunity, 82, 660–669.
10. Choi, K. H., Kumar, A., & Schweizer, H. P. (2006). A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: Application for DNA fragment transfer between chromosomes and plasmid transformation. Journal of Microbiological Methods, 64, 391–397.
11. Choi, K.-H., Gaynor, J. B., White, K. G., Lopez, C., Bosio, C. M., Karkhoff-Schweizer, R. R., & Schweizer, H. P. (2005). A Tn7-based broad-range bacterial cloning and expression system. Nature Methods, 2, 443–448.
12. Cianciotto, N. P., Cornelis, P., & Baysse, C. (2005). Impact of the bacterial type I cytochrome c maturation system on different biological processes. Molecular Microbiology, 56, 1408–1415.
13. Cruden, D. L., Wolfram, J. H., Rogers, R. D., & Gibson, D. T. (1992). Physiological properties of a Pseudomonas strain which grows with p-xylene in a two-phase (organic-aqueous) medium. Applied and Environmental Microbiology, 58, 2723–2729.
14. Dasgupta, N., Arora, S. K., & Ramphal, R. (2000). fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. Journal of Bacteriology, 182, 357–364.
15. de Lorenzo, V., & Timmis, K. N. (1994). Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods in Enzymology, 235, 386–405.
16. Domínguez-Cuevas, P., González-Pastor, J.-E., Marqués, S., Ramos, J.-L., & de Lorenzo, V. (2006). Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. The Journal of Biological Chemistry, 281, 11981–11991.
17. Dunlop, M. J., Dossani, Z. Y., Szmidt, H. L., Chu, H. C., Lee, T. S., Keasling, J. D., … Mukhopadhyay, A. (2011). Engineering microbial biofuel tolerance and export using efflux pumps. Molecular Systems Biology, 7, 487. https://doi.org/10.1038/msb.2011.21
18. Duque, E., Molina-Henares, A. J., De Torre, J., Molina-Henares, M. A., Castillo, T., Lam, J., & Ramos, J. L. (2007). Towards a genome-wide mutant library of Pseudomonas puida strain KT2440. In: Ramos, J. L., & Filloux, A. (Eds.), Pseudomonas, (pp. 227–251). Dordrecht: Springer.
19. Fernandez, M., Conde, S., De La Torre, J., Molina-Santiago, C., Ramos, J. L., & Duque, E. (2012). Mechanisms of resistance to chloramphenicol in Pseudomonas putida KT2440. Antimicrobial Agents and Chemotherapy, 56, 1001–1009.
20. Fernandez, M., Niqui-Arroyo, J. L., Conde, S., Ramos, J. L., & Duque, E. (2012). Enhanced tolerance to naphthalene and enhanced rhizoremediation performance for Pseudomonas putida KT2440 via the NAH7 catabolic plasmid. Applied and Environmental Microbiology, 78, 5104–5110.
21. Garcia, V., Godoy, P., Daniels, C., Hurtado, A., Ramos, J. L., & Segura, A. (2010). Functional analysis of new transporters involved in stress tolerance in Pseudomonas putida DOT-T1E. Environmental Microbiology Reports, 2, 389–395.
22. Gawronski, J. D., Wong, S. M. S., Giannoukos, G., Ward, D. V., & Akerley, B. J. (2009). Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proceedings of the National Academy of Sciences of the United States of America, 106, 16422–16427.
23. Glass, J. I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M. R., Maruf, M., … Venter, J. C. (2006). Essential genes of a minimal bacterium. Proceedings of the National Academy of Sciences of the United States of America, 103, 425–430.
24. Goodarzi, H., Bennett, B. D., Amini, S., Reaves, M. L., Hottes, A. K., Rabinowitz, J. D., & Tavazoie, S. (2010). Regulatory and metabolic rewiring during laboratory evolution of ethanol tolerance in E. coli. Molecular Systems Biology, 6, 378.
25. Hanahan, D. (1985). Techniques for transformation of E. coli. In D. M. Glover (Ed.), DNA cloning a Pract. approach (pp. 109–135). Oxford: United Kingdom IRL Press.
26. Heipieper, H. J., & De Bont, J. A. M. (1994). Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Applied and Environmental Microbiology, 60, 4440–4444.
27. Hensel, M., Shea, J. E., Gleeson, C., Jones, M. D., Dalton, E., & Holden, D. (1995). Simultaneous identification of bacterial virulence genes by negative selection. Science, 269, 400–403.
28. Herrero, M., Lorenzo, V. D. E., & Timmis, K. N. (1990). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. Journal of Bacteriology, 172, 6557–6567.
29. Inoue, A., Yamamoto, M., & Horikoshi, K. (1991). Pseudomonas putida which can grow in the presence of toluene. Applied and Environmental Microbiology, 57, 1560–1562.
30. Jacobs, M., Alwood, A., Thaipisuttikul, I., Spencer, D., Haugen, E., Ernst, S., … Manoil, C. (2003). Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 100, 14339–14344.
31. Jiménez, J. I., Miñambres, B., Luis, J., & Díaz, E. (2002). Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environmental Microbiology, 4, 824–841.
32. Jönsson, L. J., & Martín, C. (2016). Pretreatment of lignocellulose: Formation of inhibitory by-products and strategies for minimizing their effects. Bioresource Technology, 199, 103–112.
33. Keasling, J. D. (2010). Manufacturing molecules through metabolic enginering. Science, 330, 1355–1358.
34. Kessler, B., de Lorenzo, V., & Timmis, K. (1992). A general system to integrate lacZ fusions into the chromosomes of gram-negative eubacteria: Regulation of the Pm promoter of the TOL plasmid. Molecular and General Genetics, 233, 293–301.
35. Kieboom, J., & de Bont, J. (2001). Identification and molecular characterization of an efflux system involved in Pseudomonas putida S12 multidrug resistance. Microbiology, 147, 43–51.
36. Kim, K., Lee, S., Lee, K., & Lim, D. (1998). Isolation and characterization of toluene-sensitive mutants from the toluene-resistant bacterium Pseudomonas putida GM73. Journal of Bacteriology, 180, 3692–3696.
37. Koch, B., Jensen, L. E., & Nybroe, O. (2001). A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into gram-negative bacteria at a neutral chromosomal site. Journal of Microbiological Methods, 45, 187–195.
38. Lambertsen, L., Sternberg, C., & Molin, S. (2004). Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environmental Microbiology, 6, 726–732.
39. Langridge, G. C., Phan, M. D., Turner, D. J., Perkins, T. T., Parts, L., Haase, J., … Turner, A. K. (2009). Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Research, 19, 2308–2316.
40. Lennen, R., & Herrgård, M. J. (2014). Combinatorial strategies for improving multiple-stress resistance in industrially relevant Escherichia coli strains. Applied and Environmental Microbiology, 80, 6223–6242.
41. Lennen, R. M., Kruziki, M. A., Kumar, K., Zinkel, R. A., Burnum, K. E., Lipton, M. S., … Pfleger, B. F. (2011). Membrane stresses induced by overproduction of free fatty acids in Escherichia coli. Applied and Environmental Microbiology, 77, 8114–8128.
42. Loeschcke, A., & Thies, S. (2015). Pseudomonas putida—A versatile host for the production of natural products. Applied Microbiology and Biotechnology, 99, 197–214.
43. Lou, Z., Wang, H., Rao, S., Sun, J., Ma, C., & Li, J. (2012). P-Coumaric acid kills bacteria through dual damage mechanisms. Food Control, 25, 550–554.
44. Mack, D., Nedelmann, M., Krokotsch, A., Schwarzkopf, A., Heesemann, J., & Laufs, R. (1994). Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: Genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infection and Immunity, 62, 3244–3253.
45. Malinverni, J. C., & Silhavy, T. J. (2009). An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proceedings of the National Academy of Sciences of the United States of America, 106, 8009–8014.
46. Martínez-García, E., & de Lorenzo, V. (2011). Engineering multiple genomic deletions in gram-negative bacteria: Analysis of the multi-resistant antibiotic profile of Pseudomonas putida KT2440. Environmental Microbiology, 13, 2702–2716.
47. Martins Dos Santos, V. A. P., Heim, S., Moore, E. R. B., Strätz, M., & Timmis, K. N. (2004). Insights into the genomic basis of niche specificity of Pseudomonas putida KT2440. Environmental Microbiology, 6, 1264–1286.
48. Molina-Henares, M. A., de la Torre, J., Garcia-Salamanca, A., Molina-Henares, A. J., Herrera, M. C., Ramos, J. L., & Duque, E. (2010). Identification of conditionally essential genes for growth of Pseudomonas putida KT2440 on minimal medium through the screening of a genome-wide mutant library. Environmental Microbiology, 12, 1468–1485.
49. Mosqueda, G., & Ramos, J. L. (2000). A set of genes encoding a second toluene efflux system in Pseudomonas putida DOT-T1E is linked to the tod genes for toluene metabolism. Journal of Bacteriology, 182, 937–943.
50. Mussatto, S. I., Dragone, G., & Roberto, I. C. (2007). Ferulic and p-coumaric acids extraction by alkaline hydrolysis of brewer's spent grain. Industrial Crops and Products, 25, 231–237.
51. Nicolaou, S. A., Gaida, S. M., & Papoutsakis, E. T. (2010). A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation. Metabolic Engineering, 12, 307–331.
52. Nikel, P. I., Martínez-García, E., & de Lorenzo, V. (2014). Biotechnological domestication of pseudomonads using synthetic biology. Nature Reviews Microbiology, 12, 368–379.
53. Nour-Eldin, H. H., Geu-Flores, F., & Halkier, B. (2010). USER cloning and USER fusion: The ideal cloning techniques for small and big laboratories. Methods in Molecular Biology, 643, 185–200.
54. Poblete-Castro, I., Becker, J., Dohnt, K., dos Santos, V. M., & Wittmann, C. (2012). Industrial biotechnology of Pseudomonas putida and related species. Applied Microbiology and Biotechnology, 93, 2279–2290.
55. Ramos, J. L., Duque, E., Gallegos, M. T., Godoy, P., Ramos-González, M. I., Rojas, A., … Segura, A. (2002). Mechanisms of solvent tolerance in gram-negative bacteria. Annual Review of Microbiology, 56, 743–768.
56. Ramos, J. L., Duque, E., Godoy, P., & Segura, A. (1998). Efflux pumps involved in toluene tolerance in Pseudomonas putida DOT-T1E. Journal of Bacteriology, 180, 3323–3329.
57. Rau, M. H., Calero, P., Lennen, R. M., Long, K. S., & Nielsen, A. T. (2016). Genome-wide Escherichia coli stress response and improved tolerance towards industrially relevant chemicals. Microbial Cell Factories, 15, 176.
58. Roca, A., Rodríguez-Herva, J. J., Duque, E., & Ramos, J. L. (2008). Physiological responses of Pseudomonas putida to formaldehyde during detoxification. Microbial Biotechnology, 1, 158–169.
59. Roier, S., Zingl, F. G., Cakar, F., Durakovic, S., Kohl, P., Eichmann, T. O., … Schild, S. (2016). A novel mechanism for the biogenesis of outer membrane vesicles in gram-negative bacteria. Nature Communications, 7, 10515.
60. Rühl, J., Schmid, A., & Blank, L. M. (2009). Selected Pseudomonas putida strains able to grow in the presence of high butanol concentrations. Applied and Environmental Microbiology, 75, 4653–4656.
61. Sambrook, J., & Russel, D. W. (2000). Molecular cloning: A laboratory manual. 3rd ed. New York: Cold Spring Harboc Lab. Press.
62. Santiago, M., Matano, L. M., Moussa, S. H., Gilmore, M. S., Walker, S., & Meredith, T. C. (2015). A new platform for ultra-high density Staphylococcus aureus transposon libraries. BMC Genomics, 16, 252.
63. Santos, C. N. S., Koffas, M., & Stephanopoulos, G. (2011). Optimization of a heterologous pathway for the production of flavonoids from glucose. Metabolic Engineering, 13, 392–400.
64. Santos, P. M., Benndorf, D., & Sá-Correia, I. (2004). Insights into Pseudomonas putida KT2440 response to phenol-induced stress by quantitative proteomics. Proteomics, 4, 2640–2652.
65. Sariaslani, F. S. (2007). Development of a combined biological and chemical process for production of industrial aromatics from renewable resources. Annual Review of Microbiology, 61, 51–69.
66. Shailasree, S., Venkataramana, M., Niranjana, S. R., & Prakash, H. S. (2014). Cytotoxic effect of p-Coumaric acid on neuroblastoma, N2a cell via generation of reactive oxygen species leading to dysfunction of mitochondria inducing apoptosis and autophagy. Molecular Neurobiology, 51, 119–130.
67. Spory, A., Spory, A., Bosserhoff, A., Bosserhoff, A., von Rhein, C., von Rhein, C., … Ludwig, A. (2002). Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA. Journal of Bacteriology, 184, 3549–3559.
68. Strobel, B. W. (2001). Influence of vegetation on low-molecular-weight carboxylic acids in soil solution—A review. Geoderma, 99, 169–198.
69. Thöny-Meyer, L. (2000). Haem-polypeptide interactions during cytochrome c maturation. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1459, 316–324.
70. van Opijnen, T., & Camilli, A. (2013). Transposon insertion sequencing: A new tool for systems-level analysis of microorganisms. Nature Reviews Microbiology, 11, 435–442.
71. Verhoef, S., Ruijssenaars, H. J., de Bont, J. A. M., & Wery, J. (2007). Bioproduction of p-hydroxybenzoate from renewable feedstock by solvent-tolerant Pseudomonas putida S12. Journal of Biotechnology, 132, 49–56.
72. Verhoef, S., Wierckx, N., Westerhof, R. G. M., De Winde, J. H., & Ruijssenaars, H. J. (2009). Bioproduction of p-hydroxystyrene from glucose by the solvent-tolerant bacterium Pseudomonas putida S12 in a two-phase water-decanol fermentation. Applied and Environmental Microbiology, 75, 931–936.
73. Weber, F. J., Ooijkaas, L. P., Schemen, R. M. W., Hartmans, S., & De Bont, J. A. M. (1993). Adaptation of Pseudomonas putida S12 to high concentrations of styrene and other organic solvents. Applied and Environmental Microbiology, 59, 3502–3504.
74. Werpy, T., & Petersen, G. (2004). Top Value Added Chemicals from Biomass Volume I — Results of Screening for Potential Candidates from Sugars and Synthesis Gas Top Value Added Chemicals From Biomass Volume I: Results of Screening for Potential Candidates. Oak Ridge, TN: US Department of Energy.
75. Yang, C. H., Azad, H. R., & Cooksey, D. A. (1996). A chromosomal locus required for copper resistance, competitive fitness, and cytochrome c biogenesis in Pseudomonas fluorescens. Proceedings of the National Academy of Sciences of the United States of America, 93, 7315–7320.
76. Zomer, A., Burghout, P., Bootsma, H. J., Hermans, P. W. M., & van Hijum, S. A. F. T. (2012). Essentials: Software for rapid analysis of high throughput transposon insertion sequencing data. PLoS ONE, 7, 1–9.