Understanding biocatalyst inhibition by carboxylic acids

Frontiers in Microbiology

Volumn 4, Issue SEP, 2013, Pages

  Jarboe, Laura R ^a,b   Royce, Liam A ^a   Liu, Ping ^b  

^a Iowa State University of Science and Technology   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Acid resistance; Biocatalyst robustness; Carboxylic acid toxicity; Intracellular pH; Membrane damage; Tolerance; Transporters

Indexed keywords

CARBOXYLIC ACID; FOOD PRESERVATIVE; HOMOCYSTEINE METHYLTRANSFERASE; METHIONINE;

BIOCATALYST; CELL DISRUPTION; CELL MEMBRANE FLUIDITY; CELL MEMBRANE PERMEABILITY; CELL PH; CELLULAR STRESS RESPONSE; CYTOTOXICITY; DRUG ACCUMULATION; ESCHERICHIA COLI; FERMENTATION; HUMAN; INHIBITION KINETICS; MEMBRANE DAMAGE; METABOLIC ACTIVATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PARTITION COEFFICIENT; RENEWABLE ENERGY; RESPIRATORY FUNCTION; REVIEW; SACCHAROMYCES CEREVISIAE;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 84885403066     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00272     Document Type: Review

References (75)

1. Abbott, D. A., Knijnenburg, T. A., de Poorter, L. M. I., Reinders, M. J. T., Pronk, J. T., and van Maris, A. J. A. (2007). Generic and specific transcriptional responses to different weak organic acids in anaerobic chemostat cultures of S. cerevisiae. FEMS Yeast Res. 7, 819-833. doi:10.1111/j.1567-1364.2007.00242.x.
2. Abbott, D. A., Zelle, R. M., Pronk, J. T., and van Maris, A. J. A. (2009). Metabolic engineering of S. cerevisiae for production of carboxylic acids:current status and challenges. FEMS Yeast Res. 9, 1123-1136. doi:10.1111/j.1567-1364.2009.00537.x.
3. Al-Awqati, Q. (1999). One hundred years of membrane permeability:does Overton still rule? Nat. Cell Biol. 1, E201-E202. doi:10.1038/70230.
4. Aono, R., and Kobayashi, H. (1997). Cell surface properties of organic solvent-tolerant mutants of Escherichia coli K-12. Appl. Environ. Microbiol. 63, 3637-3642.
5. Barua, S., Yamashino, T., Hasegawa, T., Yokoyama, K., Torii, K., and Ohta, M. (2002). Involvement of surface polysaccharides in the organic acid resistance of Shiga Toxin-producing Escherichia coli O157:H7. Mol. Microbiol. 43, 629-640. doi:10.1046/j.1365-2958.2002.02768.x.
6. Cabral, M. G., Viegas, C. A., and Sa-Correia, I. (2001). Mechanisms underlying the acquisition of resistance to octanoic-acid-induced-death following exposure of S. cerevisiae to mild stress imposed by octanoic acid or ethanol. Arch. Microbiol. 175, 301-307. doi:10.1007/s002030100269.
7. Carlos Serrano-Ruiz, J., Pineda, A., Mariana Balu, A., Luque, R., Manuel Campelo, J., Angel Romero, A., et al. (2012). Catalytic transformations of biomass-derived acids into advanced biofuels. Catal. Today 195, 162-168. doi:10.1016/j.cattod.2012.01.009.
8. Carpenter, C. E., and Broadbent, J. R. (2009). External concentration of organic acid anions and pH:key independent variables for studying how organic acids inhibit growth of bacteria in mildly acidic foods. J. Food Sci. 74, R12-R15. doi:10.1111/j.1750-3841.2008.00994.x.
9. Chang, Y. Y., and Cronan, J. E. (1999). Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol. Microbiol. 33, 249-259. doi:10.1046/j.1365-2958.1999.01456.x.
10. Chotani, G., Dodge, T., Hsu, A., Kumar, M., LaDuca, R., Trimbur, D., et al. (2000). The commercial production of chemicals using pathway engineering. Biochim. Biophys. Acta 1543, 434-455. doi:10.1016/S0167-4838(00)00234-X.
11. Cipak, A., Jaganjac, M., Tehlivets, O., Kohlwein, S. D., and Zarkovic, N. (2008). Adaptation to oxidative stress induced by polyunsaturated fatty acids in yeast. Biochim. Biophys. Acta 1781, 283-287. doi:10.1016/j.bbalip.2008.03.010.
12. Comte, K., Holland, D. P., and Walsby, A. E. (2007). Changes in cell turgor pressure related to uptake of solutes by Microcystis sp. strain 8401. FEMS Microbiol. Ecol. 61, 399-405. doi:10.1111/j.1574-6941.2007.00356.x.
13. Cummings, J. H., and Macfarlane, G. T. (1991). The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol. 70, 443-459. doi:10.1111/j.1365-2672.1991.tb02739.x.
14. Desbois, A. P., and Smith, V. J. (2010). Antibacterial free fatty acids:activities, mechanisms of action and biotechnological potential. Appl. Microbiol. Biotechnol. 85, 1629-1642. doi:10.1007/s00253-009-2355-3.
15. DiezGonzalez, F., and Russell, J. B. (1997). The ability of Escherichia coli O157:H7 to decrease its intracellular pH and resist the toxicity of acetic acid. Microbiology 143, 1175-1180. doi:10.1099/00221287-143-4-1175.
16. Dunlop, M. J., Dossani, Z. Y., Szmidt, H. L., Chu, H. C., Lee, T. S., Keasling, J. D., et al. (2011). Engineering microbial biofuel tolerance and export using efflux pumps. Mol. Syst. Biol. 7, 487. doi:10.1038/msb.2011.21.
17. Evtodienko, V. Y., Kovbasnjuk, O. N., Antonenko, Y. N., and Yaguzhinsky, L. S. (1996). Effect of the alkyl chain length of monocarboxylic acid on the permeation through bilayer lipid membranes. Biochim. Biophys. Acta 1281, 245-251. doi:10.1016/0005-2736(96)00023-5.
18. Foster, J. W. (2004). Escherichia coli acid resistance:tales of an amateur acidophile. Nat. Rev. Microbiol. 2, 898-907. doi:10.1038/nrmicro1021.
19. Jarboe, L. R., Liu, P., and Royce, L. A. (2011). Engineering inhibitor tolerance for the production of biorenewable fuels and chemicals. Curr. Opin. Chem. Eng. 1, 38-42. doi:10.1016/j.coche.2011.08.003.
20. Jarboe, L. R., Zhang, X., Wang, X., Moore, J. C., Shanmugam, K. T., and Ingram, L. O. (2010). Metabolic engineering for production of biorenewable fuels and chemicals:contributions of synthetic biology. J. Biomed. Biotechnol. 2010, 761042. doi:10.1155/2010/761042.
21. Kabara, J. J., and Marshall, D. L. (2010). "Medium-chain fatty acids and esters," in Antimicrobials in Food, 3rd Edn, eds P. M. Davidson, J. N. Sofos and A. L. Branen (Boca Raton:CRC Press), 327-360.
22. Kabara, J. J., Swieczko, D. M., Truant, J. P., and Conley, A. J. (1972). Fatty acids and derivatives as antimicrobial agents. Antimicrob. Agents Chemother. 2, 23-28. doi:10.1128/AAC.2.1.23.
23. Kamp, F., and Hamilton, J. A. (2006). How fatty acids of different chain length enter and leave cells by free diffusion. Prostaglandins Leukot. Essent. Fatty Acids 75, 149-159. doi:10.1016/j.plefa.2006.05.003.
24. Kasemets, K., Kahru, A., Laht, T.-M., and Paalme, T. (2006). Study of the toxic effect of short-and medium-chain monocarboxylic acids on the growth of S. cerevisiae using the CO2-auxo-accelerostat fermentation system. Int. J. Food Microbiol. 111, 206-215. doi:10.1016/j.ijfoodmicro.2006.06.002.
25. King, T., Lucchini, S., Hinton, J. C. D., and Gobius, K. (2010). Transcriptomic analysis of Escherichia coli O157:H7 and K-12 cultures exposed to inorganic and organic acids in stationary phase reveals acidulant-and strain-specific acid tolerance responses. Appl. Environ. Microbiol. 76, 6514-6528. doi:10.1128/AEM.02392-09.
26. Legras, J. L., Erny, C., Le Jeune, C., Lollier, M., Adolphe, Y., Demuyter, C., et al. (2010). Activation of two different resistance mechanisms in S. cerevisiae upon exposure to octanoic and decanoic acids. Appl. Environ. Microbiol. 76, 7526-7535. doi:10.1128/AEM.01280-10.
27. Lennen, R. M., Braden, D. J., West, R. M., Dumesic, J. A., and Pfleger, B. F. (2010). A process for microbial hydrocarbon synthesis:overproduction of fatty acids in Escherichia coli and catalytic conversion to alkanes. Biotechnol. Bioeng. 106, 193-202. doi:10.1002/bit.22660.
28. Lennen, R. M., Kruziki, M. A., Kumar, K., Zinkel, R. A., Burnum, K. E., Lipton, M. S., et al. (2011). Membrane stresses induced by overproduction of free fatty acids in Escherichia coli. Appl. Environ. Microbiol. 77, 8114-8128. doi:10.1128/AEM.05421-11.
29. Lennen, R. M., and Pfleger, B. F. (2012). Engineering Escherichia coli to synthesize free fatty acids. Trends Biotechnol. 30, 659-667. doi:10.1016/j.tibtech.2012.09.006.
30. Lennen, R. M., and Pfleger, B. F. (2013). Modulating membrane composition alters free fatty acid tolerance in Escherichia coli. PLoS ONE 8:e54031. doi:10.1371/journal.pone.0054031.
31. Liu, J., Zhu, Y., Du, G., Zhou, J., and Chen, J. (2013a). Exogenous ergosterol protects S. cerevisiae from d-limonene stress. J. Appl. Microbiol. 114, 482-491. doi:10.1111/jam.12046.
32. Liu, P., Chernyshov, A., Najdi, T., Fu, Y., Dickerson, J., Sandmeyer, S., et al. (2013b). Membrane stress caused by octanoic acid in S. cerevisiae. Appl. Microbiol. Biotechnol. 97, 3239-3251. doi:10.1007/s00253-013-4773-5.
33. Liu, P., and Jarboe, L. R. (2012). Metabolic engineering of biocatalysts for carboxylic acids production. Comput. Struct. Biotechnol. 3, e201210011. doi:10.5936/csbj.201210011.
34. Luo, L. H., Seo, P.-S., Seo, J.-W., Heo, S.-Y., Kim, D.-H., and Kim, C. H. (2009). Improved ethanol tolerance in Escherichia coli by changing the cellular fatty acids composition through genetic manipulation. Biotechnol. Lett. 31, 1867-1871. doi:10.1007/s10529-009-0092-4.
35. Mäki-Arvela, P., Kubickova, I., Snare, M., Eränen, K., and Murzin, D. Y. (2007). Catalytic deoxygenation of fatty acids and their derivatives. Energy Fuels. 21, 30-41. doi:10.1021/ef060455v.
36. Marguet, D., Lenne, P.-F., Rigneault, H., and He, H.-T. (2006). Dynamics in the plasma membrane:how to combine fluidity and order. EMBO J. 25, 3446-3457. doi:10.1038/sj.emboj.7601204.
37. Marounek, M., Skrivanova, E., and Rada, V. (2003). Susceptibility of Escherichia coli to C-2-C-18 fatty acids. Folia Microbiol. 48, 731-735. doi:10.1007/BF02931506.
38. McDonough, V., Stukey, J., and Cavanagh, T. (2002). Mutations in erg4 affect the sensitivity of S. cerevisiae to medium-chain fatty acids. Biochim. Biophys. Acta 1581, 109-118. doi:10.1016/S1388-1981(02)00127-0.
39. Mills, T. Y., Sandoval, N. R., and Gill, R. T. (2009). Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol. Biofuels 2, 26. doi:10.1186/1754-6834-2-26.
40. Mollapour, M., Shepherd, A., and Piper, P. W. (2008). Novel stress responses facilitate S. cerevisiae growth in the presence of the monocarboxylate preservatives. Yeast 25, 169-177. doi:10.1002/yea.1576.
41. Nakanishi, N., Tashiro, K., Kuhara, S., Hayashi, T., Sugimoto, N., and Tobe, T. (2009). Regulation of virulence by butyrate sensing in enterohaemorrhagic Escherichia coli. Microbiology 155, 521-530. doi:10.1099/mic.0.023499-0.
42. Nikaido, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656. doi:10.1128/MMBR.67.4.593-656.2003.
43. Park, J. H., Jang, Y.-S., Lee, J. W., and Lee, S. Y. (2011). Escherichia coli W as a new platform strain for the enhanced production of L-valine by systems metabolic engineering. Biotechnol. Bioeng. 108, 1140-1147. doi:10.1002/bit.23044.
44. Perez, J. M., Richter, H., Loftus, S. E., and Angenent, L. T. (2013). Biocatalytic reduction of short-chain carboxylic acids into their corresponding alcohols with syngas fermentation. Biotechnol. Bioeng. 110, 1066-1077. doi:10.1002/bit.24786.
45. Piper, P., Mahe, Y., Thompson, S., Pandjaitan, R., Holyoak, C., Egner, R., et al. (1998). The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J. 17, 4257-4265. doi:10.1093/emboj/17.15.4257.
46. Piper, P. W. (1999). Yeast superoxide dismutase mutants reveal a pro-oxidant action of weak organic acid food preservatives. Free Radic. Biol. Med. 27, 1219-1227. doi:10.1016/S0891-5849(99)00147-1.
47. Rakowska, P. D., Jiang, H., Ray, S., Pyne, A., Lamarra, B., Carr, M., et al. (2013). Nanoscale imaging reveals laterally expanding antimicrobial pores in lipid bilayers. Proc. Natl. Acad. Sci. U.S.A. 110, 8918-8923. doi:10.1073/pnas.1222824110.
48. Ramos, J. L., Duque, E., Gallegos, M. T., Godoy, P., Ramos-Gonzalez, M. I., Rojas, A., et al. (2002). Mechanisms of solvent tolerance in gram-negative bacteria. Annu. Rev. Microbiol. 56, 743-768. doi:10.1146/annurev.micro.56.012302.161038.
49. Ranganathan, S., Tee, T. W., Chowdhury, A., Zomorrodi, A. R., Yoon, J. M., Fu, Y., et al. (2012). An integrated computational and experimental study for overproducing fatty acids in Escherichia coli. Metab. Eng. 14, 687-704. doi:10.1016/j.ymben.2012.08.008.
50. Ricke, S. C. (2003). Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult. Sci. 82, 632-639.
51. Roe, A. J., O'Byrne, C., McLaggan, D., and Booth, I. R. (2002). Inhibition of Escherichia coli growth by acetic acid:a problem with methionine biosynthesis and homocysteine toxicity. Microbiology 148, 2215-2222.
52. Rossi, G., Sauer, M., Porro, D., and Branduardi, P. (2010). Effect of HXT1 and HXT7 hexose transporter overexpression on wild-type and lactic acid producing S. cerevisiae cells. Microb. Cell Fact. 9, 15. doi:10.1186/1475-2859-9-15.
53. Rothen, S. A., Sauer, M., Sonnleitner, B., and Witholt, B. (1998). Biotransformation of octane by E-coli HB101[pGEc47] on defined medium:octanoate production and product inhibition. Biotechnol. Bioeng. 58, 356-365. doi:10.1002/(SICI)1097-0290(19980520)58:4<356::AID-BIT2>3.0.CO;2-I.
54. Royce, L. A., Liu, P., Stebbins, M., Hanson, B. C., and Jarboe, L. (2013). The damaging effects of short chain fatty acids on Escherichia coli membranes. Appl. Microbiol. Biotechnol. doi:10.1007/s00253-013-5113-5[Epub ahead of print].
55. Ruenwai, R., Neiss, A., Laoteng, K., Vongsangnak, W., Dalfard, A. B., Cheevadhanarak, S., et al. (2011). Heterologous production of polyunsaturated fatty acids in S. cerevisiae causes a global transcriptional response resulting in reduced proteasomal activity and increased oxidative stress. Biotechnol. J. 6, 343-356. doi:10.1002/biot.201000316.
56. Ruffing, A. M., and Jones, H. D. T. (2012). Physiological effects of free fatty acid production in genetically engineered Synechococcus elongatus PCC 7942. Biotechnol. Bioeng. 109, 2190-2199. doi:10.1002/bit.24509.
57. Russell, A. D. (1991). Mechanisms of bacterial resistance to non-antibiotics-food-additives and food and pharmaceutical preservatives. J. Appl. Bacteriol. 71, 191-201. doi:10.1111/j.1365-2672.1991.tb04447.x.
58. Russell, J. B. (1992). Another explanation for the toxicity of fermentation acids at low pH-anion accumulation versus uncoupling. J. Appl. Bacteriol. 73, 363-370. doi:10.1111/j.1365-2672.1992.tb04990.x.
59. Segura, A., Molina, L., Fillet, S., Krell, T., Bernal, P., Munoz-Rojas, J., et al. (2012). Solvent tolerance in Gram-negative bacteria. Curr. Opin. Biotechnol. 23, 415-421. doi:10.1016/j.copbio.2011.11.015.
60. +. Res. Microbiol. 159, 458-461. doi:10.1016/j.resmic.2008.04.011.
61. Shanks, B. H. (2010). Conversion of biorenewable feedstocks:new challenges in heterogeneous catalysis. Indust. Eng. Chem. Res. 49, 10212-10217. doi:10.1021/ie100487r.
62. Stratford, M., and Anslow, P. A. (1996). Comparison of the inhibitory action on S. cerevisiae of weak-acid preservatives, uncouplers, and medium-chain fatty acids. FEMS Microbiol. Lett. 142, 53-58. doi:10.1111/j.1574-6968.1996.tb08407.x.
63. Teixeira, M. C., Telo, J. P., Duarte, N. F., and Sa-Correia, I. (2004). The herbicide 2,4-dichlorophenoxyacetic acid induces the generation of free-radicals and associated oxidative stress responses in yeast. Biochem. Biophys. Res. Commun. 324, 1101-1107. doi:10.1016/j.bbrc.2004.09.158.
64. Tenreiro, S., Nunes, P. A., Viegas, C. A., Neves, M. S., Teixeira, M. C., Cabral, M. G., et al. (2002). AQR1 gene (ORF YNL065w) encodes a plasma membrane transporter of the major facilitator superfamily that confers resistance to short-chain monocarboxylic acids and quinidine in S. cerevisiae. Biochem. Biophys. Res. Commun. 292, 741-748. doi:10.1006/bbrc.2002.6703.
65. Tobe, T., Nakanishi, N., and Sugimoto, N. (2011). Activation of motility by sensing short-chain fatty acids via two steps in a flagellar gene regulatory cascade in enterohemorrhagic Escherichia coli. Infect. Immun. 79, 1016-1024. doi:10.1128/IAI.00927-10.
66. +-ATPase in the plasma membrane of S. cerevisiae is activated during growth latency in octanoic acid-supplemented medium accompanying the decrease in intracellular pH and cell viability. Appl. Environ. Microbiol. 64, 779-783.
67. Viegas, C. A., and Sa-Correia, I. (1995). Toxicity of octanoic-acid in S. cerevisiae at temperatures between 8.5 and 30°C. Enz. Microb. Technol. 17, 826-831. doi:10.1016/0141-0229(94)00111-4.
68. Walter, A., and Gutknecht, J. (1984). Monocarboxylic acid permeation through lipid bilayer membranes. J. Membr. Biol. 77, 255-264. doi:10.1007/BF01870573.
69. Wang, H.-H., Zhou, X.-R., Liu, Q., and Chen, G.-Q. (2011). Biosynthesis of polyhydroxyalkanoate homopolymers by Pseudomonas putida. Appl. Microbiol. Biotechnol. 89, 1497-1507. doi:10.1007/s00253-010-2964-x.
70. Wang, X., Yomano, L. P., Lee, J. Y., York, S. W., Zheng, H., Mullinnix, M. T., et al. (2013). Engineering furfural tolerance in Escherichia coli improves the fermentation of lignocellulosic sugars into renewable chemicals. Proc. Natl. Acad. Sci. U.S.A. 110, 4021-4026. doi:10.1073/pnas.1217958110.
71. Whitfield, C., Steers, E. J., and Weissbach, H. (1970). Purification and properties of 5-methyltetrahydropteroyltriglutamate-homocysteine transmethylase. J. Biol. Chem. 245, 390-401.
72. Yokoyama, K., Ishijima, S. A., Clowney, L., Koike, H., Aramaki, H., Tanaka, C., et al. (2006). Feast/famine regulatory proteins (FFRPs):Escherichia coli Lrp, AsnC and related archaeal transcription factors. FEMS Microbiol. Rev. 30, 89-108. doi:10.1111/j.1574-6976.2005.00005.x.
73. Zaldivar, J., and Ingram, L. O. (1999). Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol. Bioeng. 66, 203-210. doi:10.1002/(SICI)1097-0290(1999)66:4<203::AID-BIT1>3.0.CO;2-#.
74. Zhang, X., Agrawal, A., and San, K.-Y. (2012a). Improving fatty acid production in Escherichia coli through the overexpression of malonyl coA-Acyl carrier protein transacylase. Biotechnol. Prog. 28, 60-65. doi:10.1002/btpr.716.
75. Zhang, X., Li, M., Agrawal, A., and San, K.-Y. (2012b). Efficient free fatty acid production in Escherichia coli using plant acyl-ACP thioesterases. Metab. Eng. 13, 713-722. doi:10.1016/j.ymben.2011.09.007.