Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii

Biotechnology and Bioengineering

Volumn 113, Issue 4, 2016, Pages 744-753

  Lindahl, Lina ^a   Genheden, Samuel ^b,c   Eriksson, Leif A ^c   Olsson, Lisbeth ^a   Bettiga, Maurizio ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Acetic acid tolerance; Inhibitors; Lignocellulose; Membrane permeability; Molecular dynamics simulations; Myriocin

Indexed keywords

ACETIC ACID; ALUMINUM CORROSION; CELL MEMBRANES; CELLULOSIC ETHANOL; CORROSION INHIBITORS; FREE ENERGY; LIPIDS; MEMBRANES; MOLECULAR DYNAMICS; ORGANIC ACIDS; PH;

ACID TOLERANCE; LIGNOCELLULOSE; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS SIMULATIONS; MYRIOCIN;

ACID RESISTANCE;

ACETIC ACID; SPHINGOLIPID; THERMOZYMOCIDIN; ANTIFUNGAL AGENT; CULTURE MEDIUM; LIGNIN; LIGNOCELLULOSE; MONOUNSATURATED FATTY ACID;

ACIDITY; ANIMAL CELL; ANTIFUNGAL ACTIVITY; ARTICLE; BIOENGINEERING; CELL CULTURE; CELL FRACTIONATION; CELL GROWTH; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL PH; COMPUTER MODEL; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFECT; ENERGY; FLOW RATE; FUNGUS CULTURE; GROWTH INHIBITION; IN VITRO STUDY; LIPID COMPOSITION; MOLECULAR DYNAMICS; NONHUMAN; ZYGOSACCHAROMYCES BAILII; CHEMISTRY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PERMEABILITY; ZYGOSACCHAROMYCES;

ACETIC ACID; ANTIFUNGAL AGENTS; CELL MEMBRANE; CULTURE MEDIA; FATTY ACIDS, MONOUNSATURATED; LIGNIN; MOLECULAR DYNAMICS SIMULATION; PERMEABILITY; SPHINGOLIPIDS; ZYGOSACCHAROMYCES;

EID: 84959495530     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25845     Document Type: Article

References (56)

1. Allen M. 1987. Computer Simulations of Liquids. New York: Oxford University Press Inc.
2. Arneborg N, Jespersen L, Jakobsen M. 2000. Individual cells of Saccharomyces cerevisiae and Zygosaccharomyces bailii exhibit different short-term intracellular pH responses to acetic acid. Arch Microbiol 174(1-2):125-128.
3. Bayly CI, Cieplak P, Cornell WD, Kollman PA. 1993. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. J Phys Chem 97(40):10269-10280.
4. Becke AD. 1993. Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98(7):5648-5652.
5. Breslow DK, Collins SR, Bodenmiller B, Aebersold R, Simons K, Shevchenko A, Ejsing CS, Weissman JS. 2010. Orm family proteins mediate sphingolipid homeostasis. Nature 463(7284):1048-1053.
6. Chemical Computing Group Inc. 2015. Molecular Operating Environment (MOE), 2013. 08; Chemical Computing Group Inc., 1010 Sherbooke St. West, Suite \#910, Montreal, QC, Canada, H3A 2 R7.
7. Darden T, York D, Pedersen L. 1993. Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. J Chem Phys 98(12):10089-10092.
8. Dato L, Branduardi P, Passolunghi S, Cattaneo D, Riboldi L, Frascotti G, Valli M, Porro D. 2010. Advances in molecular tools for the use of Zygosaccharomyces bailii as host for biotechnological productions and construction of the first auxotrophic mutant. FEMS Yeast Research 10(7):894-908.
9. Dickey AN, Yim WS, Faller R. 2009. Using ergosterol to mitigate the deleterious effects of ethanol on bilayer structure. J Phys Chem B 113(8):2388-2397.
10. Eriksson ESE, Eriksson LA. 2011. The influence of cholesterol on the properties and permeability of hypericin derivatives in lipid membranes. J Chem Theory Comput 7(3):560-574.
11. Fernandes L, Côrte-Real M, Leao C. 1999. A peculiar behaviour for cell death induced by weak carboxylic acids in the wine spoilage yeast Zygosaccharomyces bailii. Lett Appl Microbiol 28(5):345-349.
12. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA, Jr., Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ. 2009. Gaussian 09 Revision D. 01.
13. Grossfield A. WHAM: the weighted histogram analysis method, version 2.0, http://membrane.urmc.rochester.edu/content/wham.
14. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. 1997. LINCS: A Linear constraint solver for molecular simulations. J Comput Chem 18(12):1463-1472.
15. Hess B, Kutzner C, Van Der Spoel D, Lindahl E. 2008. GRGMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4(3):435-447.
16. Huang X, Liu J, Dickson RC. 2012. Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet 8(2):1-14.
17. Hummer G. 2005. Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular dynamics simulations. New J Phys 7(34):1-14.
18. Issack BB, Peslherbe GH. 2015. Effects of cholesterol on the thermodynamics and kinetics of passive transport of water through lipid membranes. J Phys Chem B 119(29):9391-400.
19. Jakalian A, Jack DB, Bayly CI. 2002. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation. J Comput Chem 23(16):1623-1641.
20. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys 79(2):926-935.
21. Jämbeck JPM, Lyubartsev AP. 2013. Another piece of the membrane puzzle: Extending slipids further. J Chem Theory Comput 9(1):774-784.
22. Jämbeck JPM, Lyubartsev AP. 2012a. Derivation and systematic validation of a refined all-atom force field for phosphatidylcholine lipids. J Phys Chem B 116(10):3164-3179.
23. Jämbeck JPM, Lyubartsev AP. 2012b. An extension and further validation of an all-atomistic force field for biological membranes. J Chem Theory Comput 8(8):2938-2948.
24. Kendall RA, Dunning TH, Jr, Harrison RJ. 1992. Electron affinities of the first-row atoms revisited. Systematic basis sets and wave functions. J Chem Phys 96(9):6796-6806.
25. Klauda JB, Venable RM, Freites JA, O'Connor JW, Tobias DJ, Mondragon-Ramirez C, Vorobyov I, MacKerell AD, Jr, Pastor RW. 2010. Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types. J Phys Chem B 114(23):7830-7843.
26. Klose C, Surma MA, Gerl MJ, Meyenhofer F, Shevchenko A, Simons K. 2012. Flexibility of a eukaryotic lipidome-Insights from yeast lipidomics. PLoS ONE 7(4).
27. Koppram R, Tomás-Pejó E, Xiros C, Olsson L. 2014. Lignocellulosic ethanol production at high-gravity: Challenges and perspectives. Trends Biotechnol 32(1):46-53.
28. Kumar S, Rosenberg JM, Bouzida D, Swendsen RH, Kollman PA. 1992. THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J Comput Chem 13(8):1011-1021.
29. Labute P. 2010. LowModeMD - Implicit low-mode velocity filtering applied to conformational search of macrocycles and protein loops. J Chem Inform Model 50(5):792-800.
30. Lee C, Yang W, Parr RG. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 37(2):785-789.
31. Levine TP, Wiggins CAR, Munro S. 2000. Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae. Mol Biol Cell 11(7):2267-2281.
32. Lindberg L, Santos AXS, Riezman H, Olsson L, Bettiga M. 2013. Lipidomic Profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii reveals critical changes in lipid composition in response to acetic acid stress. PLoS ONE 8(9):e73936.
33. Marrink SJ, Berendsen HJC. 1994. Simulation of water transport through a lipid membrane. J Phys Chem 98(15):4155-4168.
34. Miyamoto S, Kollman PA. 1992. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13(8):952-962.
35. Neale C, Madill C, Rauscher S, Pomès R. 2013. Accelerating convergence in molecular dynamics simulations of solutes in lipid membranes by conducting a random walk along the bilayer normal. J Chem Theory Comput 9(8):3686-3703.
36. Nosé S. 1984. A unified formulation of the constant temperature molecular dynamics methods. J Chem Phys 81(1):511-519.
37. Parachin NS, Hahn-Hägerdal B, Bettiga M. 2011. A Microbial Perspective on Ethanolic Lignocellulose Fermentation. Amsterdam, The Netherlands: Elsevier. p 605-614.
38. Parrinello M, Rahman A. 1981. Polymorphic transitions in single crystals: A new molecluar dynamics method. J Appl Phys 52(12):7182-7190.
39. Piper P, Calderon CO, Hatzixanthis K, Mollapour M. 2001. Weak acid adaptation: The stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 147(10):2635-2642.
40. Rodrigues F, Sousa MJ, Ludovico P, Santos H, Côrte-Real M, Leão C. 2012. The fate of acetic acid during glucose co-metabolism by the spoilage yeast Zygosaccharomyces bailii. PLoS ONE 7(12):e52402.
41. Shimobayashi M, Oppliger W, Moes S, Jenö P, Hall MN. 2013. TORC1-regulated protein kinase Npr1 phosphorylates Orm to stimulate complex sphingolipid synthesis. Mol Biol Cell 24(6):870-881.
42. Sousa MJ, Miranda L, Côrte-Real M, Leão C. 1996. Transport of acetic acid in Zygosaccharomyces bailii: Effects of ethanol and their implications on the resistance of the yeast to acidic environments. Appl Environ Microbiol 62(9):3152-3157.
43. Sousa MJ, Rodrigues F, Côrte-Real M, Leăo C. 1998. Mechanisms underlying the transport and intracellular metabolism of acetic acid in the presence of glucose in the yeast Zygosaccharomyces bailii. Microbiology 144(3):665-670.
44. Stratford M, Steels H, Nebe-von-Caron G, Novodvorska M, Hayer K, Archer DB. 2013. Extreme resistance to weak-acid preservatives in the spoilage yeast Zygosaccharomyces bailii. Int J Food Microbiol 166(1):126-134.
45. Tomasi J, Mennucci B, Cancès E. 1999. The IEF version of the PCM solvation method: An overview of a new method addressed to study molecular solutes at the QM ab initio level. J Mol Struct THEOCHEM 464(1-3):211-226.
46. Torrie GM, Valleau JP. 1977. Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling. J Comput Phys 23(2):187-199.
47. Tribello GA, Bonomi M, Branduardi D, Camilloni C, Bussi G. 2014. PLUMED 2: New feathers for an old bird. Comput Phys Commun 185(2):604-613.
48. Wadsworth JM, Clarke DJ, McMahon SA, Lowther JP, Beattie AE, Langridge-Smith PRR, Broughton HB, Dunn TM, Naismith JH, Campopiano DJ. 2013. The chemical basis of serine palmitoyltransferase inhibition by myriocin. J Am Chem Soc 135(38):14276-14285.
49. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA. 2004. Development and testing of a general Amber force field. J Comput Chem 25(9):1157-1174.
50. Warringer J, Blomberg A. 2003. Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20(1):53-67.
51. Warth AD. 1989. Transport of benzoic and propanoic acids by Zygosaccharomyces bailii. J Gen Microbiol 135(5):1383-1390.
52. Verduyn C, Postma E, Scheffers WA, Van Dijken JP. 1992. Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8(7):501-517.
53. Woolf TB, Roux B. 1994. Conformational flexibility of o-phosphorylcholine and o-phosphorylethanolamine: A molecular dynamics study of solvation effects. J Am Chem Soc 116(13):5916-5926.
54. Wu EL, Cheng X, Jo S, Rui H, Song KC, Dávila-Contreras EM, Qi Y, Lee J, Monje-Galvan V, Venable RM, Klauda JB, Im W. 2014a. CHARMM-GUI membrane builder toward realistic biological membrane simulations. J Comput Chem 35(27):1997-2004.
55. Wu EL, Qi Y, Song KC, Klauda JB, Im W. 2014b. Preferred orientations of phosphoinositides in bilayers and their implications in protein recognition mechanisms. J Phys Chem B 118(16):4315-4325.
56. Zuehlke JM, Petrova B, Edwards CG. 2013. Advances in the control of wine spoilage by Zygosaccharomyces and Dekkera/Brettanomyces. Ann Rev Food Sci Technol 4(1):57-78.