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Mechanistic Insight into Phenolic Compounds Toxicity and State-of-the-art Strategies for Enhancing the Tolerance of Escherichia coli to Phenolic Compounds

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Abstract

Efficient use of lignocellulosic biomass is a prerequisite for sustainable biofuel production while simultaneously contributing to environmental protection. However, phenolic compounds produced during the chemical treatment of lignocellulose inhibit the growth and metabolism of microorganisms, such as Escherichia coli, which is one of the ideal strains for producing target products by microbial fermentation. To provide new ideas for studying microbial tolerance to environmental stress and providing technical support for constructing the engineering strains with high yields of phenolic compounds, this review elucidates the inhibition mechanism of phenols to E. coli. Secondly, a comprehensive and systematic review of current approaches for improving the phenolic-tolerance of E. coli is provided, including strain domestication, random mutagenesis, regulating the expression of outer membrane proteins, changing the composition of membrane fatty acids, accelerating the efflux of phenolic compounds, engineered bacterial biofloc formation, and transcriptome analysis. Finally, this review ends with some questions that still exist today, and prospective strategies are outlined for further improving the phenols-tolerance of E. coli. This review provided a theoretical basis for research into microbial tolerance to environmental stress and the development of engineered strains with high yield of phenolic compounds.

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References

  1. Bartolomé, B., M. L. Bengoechea, M. C. Gálvez, F. J. Pérez-Ilzarbe, T. Hernández, I. Estrella, and C. Gómez-Cordovés (1993) Photodiode array detection for elucidation of the structure of phenolic compounds. J. Chromatogr. A. 655: 119–125.

    Article  Google Scholar 

  2. Cheniany, M., H. Ebrahimzadeh, A. Masoudi-nejad, K. Vahdati, and C. Leslie (2010) Effect of endogenous phenols and some antioxidant enzyme activities on rooting of Persian walnut (Juglans regia L.). Afr. J. Plant Sci. 4: 479–487.

    CAS  Google Scholar 

  3. Wang, Q., K. Zhou, Y. Ning, and G. Zhao (2016) Effect of the structure of gallic acid and its derivatives on their interaction with plant ferritin. Food Chem. 213: 260–267.

    Article  CAS  PubMed  Google Scholar 

  4. Wang, J., X. Shen, J. Rey, Q. Yuan, and Y. Yan (2018) Recent advances in microbial production of aromatic natural products and their derivatives. Appl. Microbiol. Biotechnol. 102: 47–61.

    Article  CAS  PubMed  Google Scholar 

  5. Limpisophon, K. and G. Schleining (2017) Use of gallic acid to enhance the antioxidant and mechanical properties of active fish gelatin film. J. Food Sci. 82: 80–89.

    Article  CAS  PubMed  Google Scholar 

  6. Chasov, A. V. and F. V. Minibayeva (2009) Effect of exogenous phenols on superoxide production by extracellular peroxidase from wheat seedling roots. Biochemistry (Mosc.) 74: 766–774.

    Article  CAS  Google Scholar 

  7. Cao, B., K. Nagarajan, and K. C. Loh (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl. Microbiol. Biotechnol. 85: 207–228.

    Article  CAS  PubMed  Google Scholar 

  8. Liao, J. C., L. Mi, S. Pontrelli, and S. Luo (2016) Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat. Rev. Microbiol. 14: 288–304.

    Article  CAS  PubMed  Google Scholar 

  9. Peralta-Yahya, P. P., F. Zhang, S. B. del Cardayre, and J. D. Keasling (2012) Microbial engineering for the production of advanced biofuels. Nature. 488: 320–328.

    Article  CAS  PubMed  Google Scholar 

  10. Kakar, R., T. S. M. Amelia, C. C. Teng, K. Bhubalan, and A.-A. A. Amirul (2022) Biotransformation of oleochemical industry by-products to polyhydroxyalkanoate bioplastic using microbial fermentation: a review. Environ. Qual. Manag. 31: 31–46.

    Article  Google Scholar 

  11. Liu, L., X. Duan, and J. Wu (2016) L-tryptophan production in Escherichia coli improved by weakening the pta-AckA pathway. PLoS One. 11: e0158200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Liu, L., M. Bilal, X. Duan, and H. M. N. Iqbal (2019) Mitigation of environmental pollution by genetically engineered bacteria — current challenges and future perspectives. Sci. Total Environ. 667: 444–454.

    Article  CAS  PubMed  Google Scholar 

  13. Gu, H., J. Zhang, and J. Bao (2015) High tolerance and physiological mechanism of Zymomonas mobilis to phenolic inhibitors in ethanol fermentation of corncob residue. Biotechnol. Bioeng. 112: 1770–1782.

    Article  CAS  PubMed  Google Scholar 

  14. Liu, J., Q. Lin, X. Chai, Y. Luo, and T. Guo (2018) Enhanced phenolic compounds tolerance response of Clostridium beijerinckii NCIMB 8052 by inactivation of Cbei_3304. Microb. Cell Fact. 17: 35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Luo, H., Z. Liu, F. Xie, M. Bilal, and F. Peng (2021) Lignocellulosic biomass to biobutanol: toxic effects and response mechanism of the combined stress of lignin-derived phenolic acids and phenolic aldehydes to Clostridium acetobutylicum. Ind. Crops Prod. 170: 113722.

    Article  CAS  Google Scholar 

  16. Pontrelli, S., T. Y. Chiu, E. I. Lan, F. Y. Chen, P. Chang, and J. C. Liao (2018) Escherichia coli as a host for metabolic engineering. Metab. Eng. 50: 16–46.

    Article  CAS  PubMed  Google Scholar 

  17. Shin, J., Y. S. Jin, Y. C. Park, J. B. Park, Y. O. Lee, S. K. Kim, and D. H. Kweon (2021) Enhancing acid tolerance of Escherichia coli via viroporin-mediated export of protons and its application for efficient whole-cell biotransformation. Metab. Eng. 67: 277–284.

    Article  CAS  PubMed  Google Scholar 

  18. Zhu, T., D. Yao, D. Li, H. Xu, S. Jia, C. Bi, J. Cai, X. Zhu, and X. Zhang (2021) Multiple strategies for metabolic engineering of Escherichia coli for efficient production of glycolate. Biotechnol. Bioeng. 118: 4699–4707.

    Article  CAS  PubMed  Google Scholar 

  19. Guo, L., W. Diao, C. Gao, G. Hu, Q. Ding, C. Ye, X. Chen, J. Liu, and L. Liu (2020) Engineering Escherichia coli lifespan for enhancing chemical production. Nat. Catal. 3: 307–318.

    Article  CAS  Google Scholar 

  20. Liu, L., X. Duan, and J. Wu (2016) Modulating the direction of carbon flow in Escherichia coli to improve l-tryptophan production by inactivating the global regulator FruR. J. Biotechnol. 231: 141–148.

    Article  CAS  PubMed  Google Scholar 

  21. Mills, T. Y., N. R. Sandoval, and R. T. Gill (2009) Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol. Biofuels. 2: 26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fitzgerald, D. J., M. Stratford, M. J. Gasson, J. Ueckert, A. Bos, and A. Narbad (2004) Mode of antimicrobial action of vanillin against Escherichia coli, Lactobacillus plantarum and Listeria innocua. J. Appl. Microbiol. 97: 104–113.

    Article  CAS  PubMed  Google Scholar 

  23. Zaldivar, J., A. Martinez, and L. O. Ingram (1999) Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli. Biotechnol. Bioeng. 65: 24–33.

    Article  CAS  Google Scholar 

  24. Zaldivar, J., A. Martinez, and L. O. Ingram (2000) Effect of alcohol compounds found in hemicellulose hydrolysate on the growth and fermentation of ethanologenic Escherichia coli. Biotechnol. Bioeng. 68: 524–530.

    Article  CAS  PubMed  Google Scholar 

  25. Luo, H., P. Zheng, M. Bilal, F. Xie, Q. Zeng, C. Zhu, R. Yang, and Z. Wang (2020) Efficient bio-butanol production from lignocellulosic waste by elucidating the mechanisms of Clostridium acetobutylicum response to phenolic inhibitors. Sci. Total Environ. 710: 136399.

    Article  CAS  PubMed  Google Scholar 

  26. Zaldivar, J. and L. O. Ingram (1999) Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol. Bioeng. 66: 203–210.

    Article  CAS  PubMed  Google Scholar 

  27. Zhang, H. and G. Stephanopoulos (2013) Engineering E. coli for caffeic acid biosynthesis from renewable sugars. Appl. Microbiol. Biotechnol. 97: 3333–3341.

    Article  CAS  PubMed  Google Scholar 

  28. Luo, Z. W. and S. Y. Lee (2020) Metabolic engineering of Escherichia coli for the production of benzoic acid from glucose. Metab. Eng. 62: 298–311.

    Article  CAS  PubMed  Google Scholar 

  29. Lee, E. G., S. H. Yoon, A. Das, S. H. Lee, C. Li, J. Y. Kim, M. S. Choi, D. K. Oh, and S. W. Kim (2009) Directing vanillin production from ferulic acid by increased acetyl-CoA consumption in recombinant Escherichia coli. Biotechnol. Bioeng. 102: 200–208.

    Article  CAS  PubMed  Google Scholar 

  30. Cui, P., W. Zhong, Y. Qin, F. Tao, W. Wang, and J. Zhan (2020) Characterization of two new aromatic amino acid lyases from actinomycetes for highly efficient production of p-coumaric acid. Bioprocess Biosyst. Eng. 43: 1287–1298.

    Article  CAS  PubMed  Google Scholar 

  31. Barghini, P., D. Di Gioia, F. Fava, and M. Ruzzi (2007) Vanillin production using metabolically engineered Escherichia coli under non-growing conditions. Microb. Cell Fact. 6: 13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Li, Y., J. Li, B. Qian, L. Cheng, S. Xu, and R. Wang (2018) De novo biosynthesis of p-coumaric acid in E. coli with a trans-cinnamic acid 4-hydroxylase from the Amaryllidaceae plant Lycoris aurea. Molecules. 23: 3185.

    Article  CAS  PubMed Central  Google Scholar 

  33. Lv, H., Y. Zhang, J. Shao, H. Liu, and Y. Wang (2021) Ferulic acid production by metabolically engineered Escherichia coli. Bioresour. Bioprocess. 8: 70.

    Article  Google Scholar 

  34. Xu, Z., J. Kong, S. Zhang, T. Wang, and X. Liu (2020) Comparison of enzyme secretion and ferulic acid production by Escherichia coli expressing different Lactobacillus feruloyl esterases. Front. Microbiol. 11: 568716.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Pugh, S., R. McKenna, M. Osman, B. Thompson, and D. R. Nielsen (2014) Rational engineering of a novel pathway for producing the aromatic compounds p-hydroxybenzoate, protocatechuate, and catechol in Escherichia coli. Process Biochem. 49: 1843–1850.

    Article  CAS  Google Scholar 

  36. Wu, J., G. Du, J. Zhou, and J. Chen (2013) Metabolic engineering of Escherichia coli for (2S)-pinocembrin production from glucose by a modular metabolic strategy. Metab. Eng. 16: 48–55.

    Article  CAS  PubMed  Google Scholar 

  37. Watts, K. T., P. C. Lee, and C. Schmidt-Dannert (2004) Exploring recombinant flavonoid biosynthesis in metabolically engineered Escherichia coli. Chembiochem. 5: 500–507.

    Article  CAS  PubMed  Google Scholar 

  38. Qi, W. W., T. Vannelli, S. Breinig, A. Ben-Bassat, A. A. Gatenby, S. L. Haynie, and F. S. Sariaslani (2007) Functional expression of prokaryotic and eukaryotic genes in Escherichia coli for conversion of glucose to p-hydroxystyrene. Metab. Eng. 9: 268–276.

    Article  CAS  PubMed  Google Scholar 

  39. Kim, B., H. Park, D. Na, and S. Y. Lee (2014) Metabolic engineering of Escherichia coli for the production of phenol from glucose. Biotechnol. J. 9: 621–629.

    Article  CAS  PubMed  Google Scholar 

  40. Yoon, S. H., C. Li, J. E. Kim, S. H. Lee, J. Y. Yoon, M. S. Choi, W. T. Seo, J. K. Yang, J. Y. Kim, and S. W. Kim (2005) Production of vanillin by metabolically engineered Escherichia coli. Biotechnol. Lett. 27: 1829–1832.

    Article  CAS  PubMed  Google Scholar 

  41. Chen, Z., X. Shen, J. Wang, J. Wang, Q. Yuan, and Y. Yan (2017) Rational engineering of p-hydroxybenzoate hydroxylase to enable efficient gallic acid synthesis via a novel artificial biosynthetic pathway. Biotechnol. Bioeng. 114: 2571–2580.

    Article  CAS  PubMed  Google Scholar 

  42. Kambourakis, S., K. M. Draths, and J. W. Frost (2000) Synthesis of gallic acid and pyrogallol from glucose: replacing natural product isolation with microbial catalysis. J. Am. Chem. Soc. 122: 9042–9043.

    Article  CAS  Google Scholar 

  43. Verhoef, S., N. Wierckx, R. G. M. Westerhof, J. H. de Winde, and H. J. Ruijssenaars (2009) Bioproduction of p-hydroxystyrene from glucose by the solvent-tolerant bacterium Pseudomonas putida S12 in a two-phase water-decanol fermentation. Appl. Environ. Microbiol. 75: 931–936.

    Article  CAS  PubMed  Google Scholar 

  44. Wierckx, N. J. P., H. Ballerstedt, J. A. de Bont, and J. Wery (2005) Engineering of solvent-tolerant Pseudomonas putida S12 for bioproduction of phenol from glucose. Appl. Environ. Microbiol. 71: 8221–8227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nijkamp, K., R. G. Westerhof, H. Ballerstedt, J. A. de Bont, and J. Wery (2007) Optimization of the solvent-tolerant Pseudomonas putida S12 as host for the production of p-coumarate from glucose. Appl. Microbiol. Biotechnol. 74: 617–624.

    Article  CAS  PubMed  Google Scholar 

  46. Yamada, M., Y. Okada, T. Yoshida, and T. Nagasawa (2007) Biotransformation of isoeugenol to vanillin by Pseudomonas putida IE27 cells. Appl. Microbiol. Biotechnol. 73: 1025–1030.

    Article  CAS  PubMed  Google Scholar 

  47. Liu, H., X. Liu, H. Jiang, C. Liang, and Z. C. Zhang (2021) Enhanced lactic acid production from P(2)O(5)-pretreated biomass by domesticated Pediococcus pentosaceus without detoxification. Bioprocess Biosyst. Eng. 44: 2153–2166.

    Article  CAS  PubMed  Google Scholar 

  48. Wu, H., H. Wang, P. Wang, G. Zhao, H. Liu, L. Wang, X. Sun, and Z. Zheng (2021) Gradient radiation breeding and culture domestication of menaquinone producing strains. Bioprocess Biosyst. Eng. 44: 1373–1382.

    Article  CAS  PubMed  Google Scholar 

  49. Li, X.-J., R. Huang, C. Zhang, B. Luo, and D.-C. Gong (2014) Adaptation of a Saccharomyces Cerevisiae strain to lignocellulosic inhibitors by domestication. Sci. Technol. Food Ind. 7: 163–167.

    Google Scholar 

  50. Wang, M. (2018) Cultivation and domestication of activated sludge in village domestic sewage. Inn. Mong. Environ. Sci. 30: 58–59.

    Google Scholar 

  51. Yomano, L. P., S. W. York, and L. O. Ingram (1998) Isolation and characterization of ethanol-tolerant mutants of Escherichia coli KO11 for fuel ethanol production. J. Ind. Microbiol. Biotechnol. 20: 132–138.

    Article  CAS  PubMed  Google Scholar 

  52. Wang, L., B. Li, S.-P. Wang, Z.-Y. Xia, M. Gou, and Y.-Q. Tang (2021) Improving multiple stress-tolerance of a flocculating industrial Saccharomyces cerevisiae strain by random mutagenesis and hybridization. Process Biochem. 102: 275–285.

    Article  CAS  Google Scholar 

  53. Nguyen, K. N., Y. Kim, S. Maibunkaew, J. Park, M. T. Nguyen, D.-B. Oh, and O. Kwon (2021) Enhanced production of 1-deoxynojirimycin in Bacillus subtilis subsp. inaquosorum by random mutagenesis and culture optimization. Biotechnol. Bioprocess Eng. 26: 265–276.

    Article  CAS  Google Scholar 

  54. Gonzalez-Perez, D., J. Ratcliffe, S. K. Tan, M. Wong, Y. P. Yee, N. Nyabadza, J. H. Xu, T. S. Wong, and K. L. Tee (2021) Random and combinatorial mutagenesis for improved total production of secretory target protein in Escherichia coli. Sci. Rep. 11: 5290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Yoon, S. H., E. G. Lee, A. Das, S. H. Lee, C. Li, H. K. Ryu, M. S. Choi, W. T. Seo, and S. W. Kim (2007) Enhanced vanillin production from recombinant E. coli using NTG mutagenesis and adsorbent resin. Biotechnol. Prog. 23: 1143–1148.

    PubMed  Google Scholar 

  56. Yi, X., L. Lin, J. Mei, and W. Wang (2021) Transporter proteins in Zymomonas mobilis contribute to the tolerance of lignocellulose-derived phenolic aldehyde inhibitors. Bioprocess Biosyst. Eng. 44: 1875–1882.

    Article  CAS  PubMed  Google Scholar 

  57. Mitra, A., S. Chatterjee, S. Kataki, R. P. Rastogi, and D. K. Gupta (2021) Bacterial tolerance strategies against lead toxicity and their relevance in bioremediation application. Environ. Sci. Pollut. Res. Int. 28: 14271–14284.

    Article  CAS  PubMed  Google Scholar 

  58. Randhawa, A., N. Pasari, T. Sinha, M. Gupta, A. M. Nair, O. A. Ogunyewo, S. Verma, P. K. Verma, and S. S. Yazdani (2021) Blocking drug efflux mechanisms facilitate genome engineering process in hypercellulolytic fungus, Penicillium funiculosum NCIM1228. Biotechnol. Biofuels. 14: 31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Segura, A., L. Molina, S. Fillet, T. Krell, P. Bernal, J. Muñoz-Rojas, and J. L. Ramos (2012) Solvent tolerance in Gramnegative bacteria. Curr. Opin. Biotechnol. 23: 415–421.

    Article  CAS  PubMed  Google Scholar 

  60. Bafna, J. A., E. Sans-Serramitjana, S. Acosta-Gutiérrez, I. V. Bodrenko, D. Hörömpöli, A. Berscheid, H. Brötz-Oesterhelt, M. Winterhalter, and M. Ceccarelli (2020) Kanamycin uptake into Escherichia coli is facilitated by OmpF and OmpC porin channels located in the outer membrane. ACS Infect. Dis. 6: 1855–1865.

    Article  CAS  PubMed  Google Scholar 

  61. Chetri, S., M. Singha, D. Bhowmik, K. Nath, D. D. Chanda, A. Chakravarty, and A. Bhattacharjee (2019) Transcriptional response of OmpC and OmpF in Escherichia coli against differential gradient of carbapenem stress. BMC Res. Notes. 12: 138.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Begic, S. and E. A. Worobec (2006) Regulation of Serratia marcescens ompF and ompC porin genes in response to osmotic stress, salicylate, temperature and pH. Microbiology (Reading). 152: 485–491.

    Article  CAS  PubMed  Google Scholar 

  63. Zhang, D. F., H. Li, X. M. Lin, S. Y. Wang, and X. X. Peng (2011) Characterization of outer membrane proteins of Escherichia coli in response to phenol stress. Curr. Microbiol. 62: 777–783.

    Article  CAS  PubMed  Google Scholar 

  64. Goose, J. E. and M. S. P. Sansom (2013) Reduced lateral mobility of lipids and proteins in crowded membranes. PLoS Comput. Biol. 9: e1003033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Guzmán-Flores, J. E., L. Steinemann-Hernández, L. E. González de la Vara, M. Gavilanes-Ruiz, T. Romeo, A. F. Alvarez, and D. Georgellis (2019) Proteomic analysis of Escherichia coli detergent-resistant membranes (DRM). PLoS One. 14: e0223794.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yin, N., G. Zhu, Q. Luo, J. Liu, X. Chen, and L. Liu (2020) Engineering of membrane phospholipid component enhances salt stress tolerance in Saccharomyces cerevisiae. Biotechnol. Bioeng. 117: 710–720.

    Article  CAS  PubMed  Google Scholar 

  67. Liu, Y., Q. Liu, A. Krivoruchko, S. Khoomrung, and J. Nielsen (2020) Engineering yeast phospholipid metabolism for de novo oleoylethanolamide production. Nat. Chem. Biol. 16: 197–205.

    Article  CAS  PubMed  Google Scholar 

  68. Keweloh, H., R. Diefenbach, and H. J. Rehm (1991) Increase of phenol tolerance of Escherichia coli by alterations of the fatty acid composition of the membrane lipids. Arch. Microbiol. 157: 49–53.

    Article  CAS  PubMed  Google Scholar 

  69. Satoh, S., M. Ozaki, S. Matsumoto, T. Nabatame, M. Kaku, T. Shudo, M. Asayama, and S. Chohnan (2020) Enhancement of fatty acid biosynthesis by exogenous acetyl-CoA carboxylase and pantothenate kinase in Escherichia coli. Biotechnol. Lett. 42: 2595–2605.

    Article  CAS  PubMed  Google Scholar 

  70. Cao, Y., J. Yang, M. Xian, X. Xu, and W. Liu (2010) Increasing unsaturated fatty acid contents in Escherichia coli by coexpression of three different genes. Appl. Microbiol. Biotechnol. 87: 271–280.

    Article  CAS  PubMed  Google Scholar 

  71. Liu, P., A. Chernyshov, T. Najdi, Y. Fu, J. Dickerson, S. Sandmeyer, and L. Jarboe (2013) Membrane stress caused by octanoic acid in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 97: 3239–3251.

    Article  CAS  PubMed  Google Scholar 

  72. Tan, Z., J. M. Yoon, D. R. Nielsen, J. V. Shanks, and L. R. Jarboe (2016) Membrane engineering via trans unsaturated fatty acids production improves Escherichia coli robustness and production of biorenewables. Metab. Eng. 35: 105–113.

    Article  CAS  PubMed  Google Scholar 

  73. Tan, Z., P. Khakbaz, Y. Chen, J. Lombardo, J. M. Yoon, J. V. Shanks, J. B. Klauda, and L. R. Jarboe (2017) Engineering Escherichia coli membrane phospholipid head distribution improves tolerance and production of biorenewables. Metab. Eng. 44: 1–12.

    Article  CAS  PubMed  Google Scholar 

  74. Jones, H. E., I. B. Holland, A. Jacq, T. Wall, and A. K. Campbell (2003) Escherichia coli lacking the AcrAB multidrug efflux pump also lacks nonproteinaceous, PHB-polyphosphate Ca2+ channels in the membrane. Biochim. Biophys. Acta. 1612: 90–97.

    Article  CAS  PubMed  Google Scholar 

  75. Rosenberg, E. Y., D. Ma, and H. Nikaido (2000) AcrD of Escherichia coli is an aminoglycoside efflux pump. J. Bacteriol. 182: 1754–1756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Licandro-Seraut, H., C. Roussel, G. Perpetuini, P. Gervais, and J. F. Cavin (2013) Sensitivity to vinyl phenol derivatives produced by phenolic acid decarboxylase activity in Escherichia coli and several food-borne Gram-negative species. Appl. Microbiol. Biotechnol. 97: 7853–7864.

    Article  CAS  PubMed  Google Scholar 

  77. Alekshun, M. N. and S. B. Levy (1999) Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. J. Bacteriol. 181: 4669–4672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Hächler, H., S. P. Cohen, and S. B. Levy (1991) marA, a regulated locus which controls expression of chromosomal multiple antibiotic resistance in Escherichia coli. J. Bacteriol. 173: 5532–5538.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Van Dyk, T. K., L. J. Templeton, K. A. Cantera, P. L. Sharpe, and F. S. Sariaslani (2004) Characterization of the Escherichia coli AaeAB efflux pump: a metabolic relief valve? J. Bacteriol. 186: 7196–7204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kurgan, G., L. A. Panyon, Y. Rodriguez-Sanchez, E. Pacheco, L. M. Nieves, R. Mann, D. R. Nielsen, and X. Wang (2019) Bioprospecting of native efflux pumps to enhance furfural tolerance in ethanologenic Escherichia coli. Appl. Environ. Microbiol. 85: e02985–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Wang, S., X. Sun, and Q. Yuan (2018) Strategies for enhancing microbial tolerance to inhibitors for biofuel production: a review. Bioresour. Technol. 258: 302–309.

    Article  CAS  PubMed  Google Scholar 

  82. Turner, W. J. and M. J. Dunlop (2015) Trade-offs in improving biofuel tolerance using combinations of efflux pumps. ACS Synth. Biol. 4: 1056–1063.

    Article  CAS  PubMed  Google Scholar 

  83. Lee, K. and S. S. Yoon (2017) Pseudomonas aeruginosa biofilm, a programmed bacterial life for fitness. J. Microbiol. Biotechnol. 27: 1053–1064.

    Article  CAS  PubMed  Google Scholar 

  84. Valentini, M. and A. Filloux (2016) Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. J. Biol. Chem. 291: 12547–12555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Li, Y., P. Xiao, Y. Wang, and Y. Hao (2020) Mechanisms and control measures of mature biofilm resistance to antimicrobial agents in the clinical context. ACS Omega. 5: 22684–22690.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Singh, R., D. Paul, and R. K. Jain (2006) Biofilms: implications in bioremediation. Trends Microbiol. 14: 389–397.

    Article  CAS  PubMed  Google Scholar 

  87. Farhadian, M., D. Duchez, C. Vachelard, and C. Larroche (2008) Monoaromatics removal from polluted water through bioreactors-a review. Water Res. 42: 1325–1341.

    Article  CAS  PubMed  Google Scholar 

  88. Wu, Y., Y. Ding, Y. Cohen, and B. Cao (2015) Elevated level of the second messenger c-di-GMP in Comamonas testosteroni enhances biofilm formation and biofilm-based biodegradation of 3-chloroaniline. Appl. Microbiol. Biotechnol. 99: 1967–1976.

    Article  CAS  PubMed  Google Scholar 

  89. Jia, X., S. Zhang, J. Li, J. Xia, R. Yao, X. Zhao, B. Wu, F. Bai, and Y. Xiao (2020) Engineered bacterial biofloc formation enhancing phenol removal and cell tolerance. Appl. Microbiol. Biotechnol. 104: 1187–1199.

    Article  CAS  PubMed  Google Scholar 

  90. Li, Q., X. Q. Zhao, A. K. Chang, Q. M. Zhang, and F. W. Bai (2012) Ethanol-induced yeast flocculation directed by the promoter of TPS1 encoding trehalose-6-phosphate synthase 1 for efficient ethanol production. Metab. Eng. 14: 1–8.

    Article  CAS  PubMed  Google Scholar 

  91. Wackett, L. P. (2003) Pseudomonas putida—a versatile biocatalyst. Nat. Biotechnol. 21: 136–138.

    Article  CAS  PubMed  Google Scholar 

  92. Wierckx, N. J., H. Ballerstedt, J. A. de Bont, and J. Wery (2005) Engineering of solvent-tolerant Pseudomonas putida S12 for bioproduction of phenol from glucose. Appl. Environ. Microbiol. 71: 8221–8227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Wery, J., D. I. Mendes da Silva, and J. A. de Bont (2000) A genetically modified solvent-tolerant bacterium for optimized production of a toxic fine chemical. Appl. Microbiol. Biotechnol. 54: 180–185.

    Article  CAS  PubMed  Google Scholar 

  94. Verhoef, S., H. J. Ruijssenaars, J. A. de Bont, and J. Wery (2007) Bioproduction of p-hydroxybenzoate from renewable feedstock by solvent-tolerant Pseudomonas putida S12. J. Biotechnol. 132: 49–56.

    Article  CAS  PubMed  Google Scholar 

  95. Ramos, J. L., E. Duque, M. T. Gallegos, P. Godoy, M. I. Ramos-Gonzalez, A. Rojas, W. Teran, and A. Segura (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu. Rev. Microbiol. 56: 743–768.

    Article  CAS  PubMed  Google Scholar 

  96. Ramos, J. L., E. Duque, J. J. Rodríguez-Herva, P. Godoy, A. Haïdour, F. Reyes, and A. Fernández-Barrero (1997) Mechanisms for solvent tolerance in bacteria. J. Biol. Chem. 272: 3887–3890.

    Article  CAS  PubMed  Google Scholar 

  97. Zhang, X.-Y., T.-T. Li, Y.-R. Liu, S.-S. Geng, A.-L. Luo, M.-S. Jiang, X.-W. Liang, J.-H. Shang, K.-H. Lu, and X.-G. Yang (2021) Transcriptome analysis revealed differences in the microenvironment of spermatogonial stem cells in seminiferous tubules between pre-pubertal and adult buffaloes. Reprod. Domest. Anim. 56: 629–641.

    Article  CAS  PubMed  Google Scholar 

  98. Lv, H., M. Kim, S. Park, K. Baek, H. Oh, J. E. W. Polle, and E. S. Jin (2021) Comparative transcriptome analysis of short-term responses to salt and glycerol hyperosmotic stress in the green alga Dunaliella salina. Algal Res. 53: 102147.

    Article  Google Scholar 

  99. Gu, P., J. Kang, F. Yang, Q. Wang, Q. Liang, and Q. Qi (2013) The improved L-tryptophan production in recombinant Escherichia coli by expressing the polyhydroxybutyrate synthesis pathway. Appl. Microbiol. Biotechnol. 97: 4121–4127.

    Article  CAS  PubMed  Google Scholar 

  100. Dong, H., W. Zhang, Q. Xuan, Y. Zhou, S. Zhou, J. Huang, and P. Wang (2021) Binding peptide-guided immobilization of lipases with significantly improved catalytic performance using Escherichia coli BL21(DE3) biofilms as a platform. ACS Appl. Mater. Interfaces. 13: 6168–6179.

    Article  CAS  PubMed  Google Scholar 

  101. Müller, C., L. Petruschka, H. Cuypers, G. Burchhardt, and H. Herrmann (1996) Carbon catabolite repression of phenol degradation in Pseudomonas putida is mediated by the inhibition of the activator protein PhlR. J. Bacteriol. 178: 2030–2036.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Yang, J., T. Gao, Y. Zhang, S. Wang, H. Li, S. Li, and S. Wang (2019) Degradation of the phenolic β-ether lignin model dimer and dyes by dye-decolorizing peroxidase from Bacillus amyloliquefaciens. Biotechnol. Lett. 41: 1015–1021.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work is supported by the National Natural Science Foundation of China (21808075), and the Natural Science Foundation of Jiangsu Province (BK20170459).

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Authors and Affiliations

  1. School of Life Science and Food Engineering, Huaiyin Institute of Technology, Huaian, 223003, China

    Lina Liu, Xiaolong Ma, Muhammad Bilal, Linlin Wei, Shijie Tang, Hongzhen Luo & Yuping Zhao

  2. College of Light Industry and Food Engineering, Nanjing Forestry University, Nanjing, Jiangsu, 210037, China

    Xuguo Duan

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  1. Lina Liu
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  2. Xiaolong Ma
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  3. Muhammad Bilal
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  4. Linlin Wei
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  5. Shijie Tang
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  6. Hongzhen Luo
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  7. Yuping Zhao
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  8. Xuguo Duan
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Contributions

LL conceived and designed research. XM, LW, and ST collected data. YZ, HL, and XD analyzed data. LL and MB wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Lina Liu.

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This article does not contain any studies with human participants or animals performed by any authors.

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Liu, L., Ma, X., Bilal, M. et al. Mechanistic Insight into Phenolic Compounds Toxicity and State-of-the-art Strategies for Enhancing the Tolerance of Escherichia coli to Phenolic Compounds. Biotechnol Bioproc E 27, 533–542 (2022). https://doi.org/10.1007/s12257-022-0019-7

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  • DOI: https://doi.org/10.1007/s12257-022-0019-7

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