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Membrane Homeostasis in Bacteria upon pH Challenge

  • Christian Sohlenkamp
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Bacteria are frequently exposed to acid stress. In order to survive these unfavorable conditions, they have evolved a set of resistance mechanisms, which include the pumping of protons out of the cytoplasm, the production of ammonia, proton-consuming decarboxylation reactions, and modifications of the membrane lipid composition. In this chapter, I will discuss the changes in membrane composition that have been described in bacteria to be part of the adaptation to acid stress conditions. The cytoplasmic membrane is a major barrier to proton influx in acid-treated cells. However, there is no single one membrane adaptation used by all bacteria in response to acid stress. Rather, different bacteria seem to use different strategies to adjust their membrane lipid composition in response to an increase in proton concentration.

Notes

Acknowledgments

Work in the laboratory was supported by grants to C.S. from SEP-CONACyT (237713) and PAPIIT-UNAM (IN202413, IN208116).

References

  1. Arendt W, Groenewold MK, Hebecker S, Dickschat JS, Moser J (2013) Identification and characterization of a periplasmic aminoacyl-phosphatidylglycerol hydrolase responsible for Pseudomonas aeruginosa lipid homeostasis. J Biol Chem 288:24717–24730CrossRefGoogle Scholar
  2. Basconcillo LS, Zaheer R, Finan TM, McCarry BE (2009) Cyclopropane fatty acyl synthase in Sinorhizobium meliloti. Microbiology-SGM 155:373–385CrossRefGoogle Scholar
  3. Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci U S A 90:6091–6094CrossRefGoogle Scholar
  4. Broadbent JR, Larsen RL, Deibel V, Steele JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol 192:2445–2458CrossRefGoogle Scholar
  5. Brown JL, Ross T, McMeekin TA, Nichols PD (1997) Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int J Food Microbiol 37:163–173CrossRefGoogle Scholar
  6. Chang Y-Y, Cronan JE Jr (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33:249–259CrossRefGoogle Scholar
  7. Ernst CM, Staubitz P, Mishra NN, Yang S-J, Hornig G, Kalbacher H, Bayer AS, Kraus D, Peschel A (2009) The bacterial defensing resistance protein MprF consists of separable domains for lipid lysinylation and antimicrobial peptide repulsion. PLoS Pathog 5(11):e1000660.  https://doi.org/10.1371/journal.ppat.1000660CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fozo EM, Quivey RG Jr (2004a) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70:929–936CrossRefGoogle Scholar
  9. Fozo EM, Quivey RG Jr (2004b) The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J Bacteriol 186:4152–4158CrossRefGoogle Scholar
  10. Fozo EM, Kajfasz JK, Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238:291–295CrossRefGoogle Scholar
  11. Gibbons HS, Lin S, Cotter RJ, Raetz CRH (2000) Oxygen requirement for the biosynthesis of the S-2-hydroxymyristate moiety in Salmonella typhimurium lipid A. Function of LpxO, a new Fe(II)/alpha-ketoglutarate-dependent dioxygenase homologue. J Biol Chem 275:32940–32949CrossRefGoogle Scholar
  12. Gibbons HS, Reynolds CM, Guan Z, Raetz CRH (2008) An inner membrane dioxygenase that generates the 2-hydroxymyristate moiety of Salmonella lipid A. Biochemistry 47:2814–2825CrossRefGoogle Scholar
  13. Giotis ES, McDowell DA, Blair IS, Wilkinson BJ (2007) Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes. Appl Environ Microbiol 73:997–1001CrossRefGoogle Scholar
  14. Gónzalez-Silva N, López-Lara IM, Reyes-Lamothe R, Taylor AM, Sumpton D, Thomas-Oates J, Geiger O (2011) The dioxygenase-encoding olsD gene from Burkholderia cenocepacia causes the hydroxylation of the amide-linked fatty acyl moiety of ornithine- membrane lipids. Biochemistry 50:6396–6408CrossRefGoogle Scholar
  15. Haque M, Hirai Y, Yokota K, Mori N, Jahan I, Ito H, Hotta H, Yano I, Kanemasa Y, Ogawa K (1996) Lipid profile of Helicobacter spp.: presence of cholesteryl glucoside as a characteristic feature. J Bacteriol 178:2065–2070CrossRefGoogle Scholar
  16. Hellweg C, Pühler A, Weidner S (2009) The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acid pH. BMC Microbiol 9:37CrossRefGoogle Scholar
  17. Henderson JC, Zimmerman SM, Crofts AA, Boll JM, Kuhns LG, Herrera CM, Trent SM (2016) The power of asymmetry: architecture and assembly of the gram-negative outer membrane lipid bilayer. Annu Rev Microbiol 70:755–778CrossRefGoogle Scholar
  18. Horbach S, Neuss B, Sahm H (1991) Effect of azasqualene on hopanoid biosynthesis and ethanol tolerance of Zymomonas mobilis. FEMS Microbiol Lett 79:347–250CrossRefGoogle Scholar
  19. Houtsmuller UM, van Deenen LL (1965) On the amino acid esters of phosphatidyl glycerol from bacteria. Biochim Biophys Acta 106:564–576CrossRefGoogle Scholar
  20. Kang HW, Wirawan IG, Kojima M (1994) Cellular localization and functional analysis of the protein encoded by the chromosomal virulence gene (acvB) of Agrobacterium tumefaciens. Biosci Biotechnol Biochem 58:2024–2032CrossRefGoogle Scholar
  21. Kanjee U, Houry WA (2013) Mechanisms of acid resistance in Escherichia coli. Annu Rev Microbiol 67:65–81CrossRefGoogle Scholar
  22. Kerger BD, Nichols PD, Antworth CP, Sand W, Bock E, Cox JC, Langworthy TA, White DC (1986) Signature fatty acids in the polar lipids of acid-producing Thiobacillus spp.: methoxy, cyclopropyl, alpha-hydroxy-cyclopropyl and branched and normal monoenoic fatty acid. FEMS Microbiol Ecol 38:67–77CrossRefGoogle Scholar
  23. Kim BH, Kim S, Kim HG, Lee J, Lee IS, Park YK (2005) The formation of cyclopropane fatty acids in Salmonella enterica serovar typhimurium. Microbiol-SGM 151:209–218CrossRefGoogle Scholar
  24. Klein S, Lorenzo C, Hoffmann S, Walther JM, Storbeck S, Piekarski T, Tindall BJ, Wray V, Nimtz M, Moser J (2009) Adaptation of Pseudomonas aeruginosa to various conditions includes tRNA-dependent formation of alanyl-phosphatidylglycerol. Mol Microbiol 71:551–565CrossRefGoogle Scholar
  25. Kulkarni G, Busset N, Molinaro A, Gargani D, Chaintreuil C, Silipo A, Giraud E, Newmann DK (2015) Specific hopanoid classes differentially affect free-living and symbiotic states of Bradyrhizobium diazoefficiens. MBio 6:e01251-15CrossRefGoogle Scholar
  26. Levin RA (1971) Fatty acids of Thiobacillus thiooxidans. J Bacteriol 108:992–995PubMedPubMedCentralGoogle Scholar
  27. Lund P, Tramonti A, De Biase D (2014) Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev 38:1091–1125CrossRefGoogle Scholar
  28. MacGilvray ME, Lapek JD, Friedman AE, Quivey RG Jr (2012) Cardiolipin biosynthesis in Streptococcus mutans is regulated by response to external pH. Microbiol-SGM 158:2133–2143CrossRefGoogle Scholar
  29. Martinić M, Hoare A, Contreras I, Álvarez SA (2011) Contribution of the lipopolysaccharide to resistance of Shigella flexneri 2a to extreme acidity. PLoS One 6:e25557CrossRefGoogle Scholar
  30. Mizoguchi T, Tsukatani Y, Harada J, Takasaki S, Yoshitomi T, Tamiaki H (2013) Cyclopropane-ring formation in the acyl groups of chlorosome glycolipids is crucial for acid resistance of green bacterial antenna systems. Bioorg Med Chem 21:3689–3694CrossRefGoogle Scholar
  31. Mykytczuk NCS, Trevors JT, Ferroni GD, Leduc LG (2010) Cytoplasmic membrane fluidity and fatty acod composition of Acidothiobacillus ferrooxidans in response to pH stress. Extremophiles 14:427–441CrossRefGoogle Scholar
  32. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656CrossRefGoogle Scholar
  33. Ogawa S, Tachimoto H, Kaga T (2010) Elevation of ceramide in Acetobacter malorum S24 by low pH stress and high temperature stress. J Biosci Bioeng 109:32–36CrossRefGoogle Scholar
  34. Palacios-Chaves L, Zuñiga-Ripa A, Gutiérrez A, Gil-Ramírez Y, Conde-Álvarez R, Moriyón I, Iriarte M (2012) Identification and functional analysis of the cyclopropane fatty acid synthase of Brucella abortus. Microbiology 158:1037–1044CrossRefGoogle Scholar
  35. Parsons JB, Rock CO (2013) Bacterial lipids: metabolism and membrane homeostasis. Prog Lipid Res 52:249–276CrossRefGoogle Scholar
  36. Patton JL, Srinivasan B, Dickson RC, Lester RL (1992) Phenotypes of sphingolipid-dependent strains of Saccharomyces cerevisiae. J Bacteriol 174:7180–7184CrossRefGoogle Scholar
  37. Pini C-V, Bernal P, Godoy P, Ramos J-L, Segura A (2009) Cyclopropane fatty acids are involved in organic solvent tolerance but not in acid stress resistance in Pseudomonas putida DOT-T1E. Microb Biotechnol 2:253–261CrossRefGoogle Scholar
  38. Poger D, Mark AE (2015) A ring to rule them all: the effect of cyclopropane fatty acids on the fluidity of lipid bilayers. J Phys Chem B 119:5487–5495CrossRefGoogle Scholar
  39. Poralla K, Hartner T, Kannenberg E (1984) Effect of termperature and pH on the hopanoid content of Bacillus acidocaldarius. FEMS Microbiol Lett 23:253–256CrossRefGoogle Scholar
  40. Poralla K, Muth G, Hartner T (2000) Hopanoids are formed during transition from substrate to aerial hyphae in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 189:93–95CrossRefGoogle Scholar
  41. Rojas-Jiménez K, Sohlenkamp C, Geiger O, Martínez-Romero E, Werner D, Vinuesa P (2005) A ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Mol Plant-Microbe Interact 18:1175–1185CrossRefGoogle Scholar
  42. Sáenz JP, Sezgin E, Schwille P, Simons K (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad of Sci USA 109:14236–14240CrossRefGoogle Scholar
  43. Sáenz JP, Grosser D, Bradley AS, Lagny TJ, Lavrynenko O, Broda M, Simons K (2015) Hopanoids as functional analogues of cholesterol in bacterial membranes. Proc Natl Acad Sci U S A 112:11971–11976CrossRefGoogle Scholar
  44. Schmerk CL, Bernards MA, Valvano MA (2011) Hopanoid production is required for low-pH tolerance, antimicrobial resistance, and motility in Burkholderia cenocepacia. J Bacteriol 193:6712–6723CrossRefGoogle Scholar
  45. Seipke RF, Loria R (2009) Hopanoids are not essential for growth of Streptomyces scabies 87-22. J Bacteriol 191:5216–5223CrossRefGoogle Scholar
  46. Shabala L, Ross T (2008) Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+. Res Microbiol 159:458–461CrossRefGoogle Scholar
  47. Silipo A, Vitiello G, Gully D, Sturiale L, Chaintreuil C, Fardoux J, Gargani D, Lee H-I, Kulkarni G, Busset N, Marchetti R, Palmigiano A, Moll H, Engel R, Lanzetta R, Paduano L, Parrilli M, Chang W-S, Holst O, Newman DK, Garozzo D, D’Errico G, Giraud E, Molinaro A (2014) Covalently linked hopanoid-lipid a improves outer-membrane resistance of a Bradyrhizobium symbiont of legumes. Nature Comm 5:5106.  https://doi.org/10.1038/ncomms6106CrossRefGoogle Scholar
  48. Slavetinsky CJ, Peschel A, Ernst CM (2012) Alabyl-phosphatidylglycerol and lysyl-phosphatidylglycerol are translocated by the same MprF flippases and have similar capacities to protect against the antibiotic daptomycin in Staphylococcus aureus. Antimicrob Ag Chemother 56:3492–3497CrossRefGoogle Scholar
  49. Slavetinsky C, Kuhn S, Peschel A (2016) Bacterial aminoacyl phospholipids- biosynthesis and role in basic cellular processes and pathogenicity. Biochim Biophys Acta.  https://doi.org/10.1016/j.bbalip.2016.11.013CrossRefGoogle Scholar
  50. Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 40:133–159CrossRefGoogle Scholar
  51. Sohlenkamp C, Galindo-Lagunas KA, Guan Z, Vinuesa P, Robinson S, Thomas-Oates J, Raetz CRH, Geiger O (2007) The lipid lysyl-phosphatidylglycerol in is present in membranes of Rhizobium tropici CIAT899 and confers increased resistance to polymyxin B under acidic growth conditions. Mol Plant-Microbe Interact 20:1421–1430CrossRefGoogle Scholar
  52. Vences-Guzmán MA, Guan Z, Ormeño-Orrillo E, González-Silva N, López-Lara IM, Martínez-Romero E, Geiger O, Sohlenkamp C (2011) Hydroxylated ornithine lipids increase stress tolerance in Rhizobium tropici CIAT899. Mol Microbiol 79:1496–1514CrossRefGoogle Scholar
  53. Vences-Guzmán MA, Guan Z, Escobedo-Hinojosa WI, Bermúdez-Barrientes JR, Geiger O, Sohlenkamp C (2015) Discovery of a bifunctional acyltransferase responsible for ornithine lipid synthesis in Serratia proteamaculans. Environ Microbiol 17:1487–1496CrossRefGoogle Scholar
  54. Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martínez-Romero E, Werner D (2003) Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol Plant-Microbe Interact 16:159–168CrossRefGoogle Scholar
  55. Welander PV, Hunter RC, Zhang L, Sessions AL, Summons RE, Newman DK (2009) Hopanoids play a role in membrane integrity and pH homeostasis in Rhodopseudomonas palustris TIE-1. J Bacteriol 191:6145–6156CrossRefGoogle Scholar
  56. Zhang Y-M, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Centro de Ciencias GenómicasUniversidad Nacional Autónoma de MéxicoCuernavacaMexico

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