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Biogenesis of Fatty Acids, Lipids and Membranes pp 1–13Cite as

Regulation of Membrane Lipid Homeostasis in Bacteria upon Temperature Change

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Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

Abstract

Bacteria precisely remodel the fluidity of their membrane bilayer via the incorporation of proportionally more unsaturated fatty acids (or fatty acids with analogous properties, such as branched-chain fatty acids) as growth temperature decreases. This process, termed homeoviscous adaptation, is suited to disrupt the order of the lipid bilayer and optimizes the performance of a large array of cellular physiological processes at the new temperature. As such, microbes have developed molecular strategies to sense changes in membrane fluidity, provoked by a decrease in environmental temperature, and initiate cellular responses that upregulate the biosynthesis of either unsaturated, terminally branched, or shorter-chain fatty acids. In this review we describe some of the basic molecular strategies that bacteria use to sense temperature. While the activities of all biomolecules are altered as a function of temperature, the thermosensors we focus on here are molecules whose temperature sensitivity provides information about the thermal environment that is used to trigger an appropriate adjustment of membrane architecture. We also discuss selected examples of membrane and lipopolysaccharide remodeling induced by cold that involves changes in the activity of fatty acid biosynthetic enzymes or the expression of acyltransferases that modify the lipid A.

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References

  • Altabe SG, Mansilla MC, de Mendoza D (2013) Remodeling of membrane lipids by bacterial desaturases. In: Ntambi JM (ed) Stearoyl-CoA desaturase genes in lipid metabolism. Springer, New York, pp 209–231

    Chapter  Google Scholar 

  • Annous BA, Becker LA, Bayles DO, Labeda DP, Wilkinson BJ (1997) Critical role of anteiso-C15:0 fatty acid in the growth of at low temperatures. Appl Environ Microbiol 63:3887–3894

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beckering CL, Steil L, Weber MH, Volker U, Marahiel MA (2002) Genome wide transcriptional analysis of the cold shock response in Bacillus subtilis. J Bacteriol 184:6395–6402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chazarreta Cifré L, Alemany M, de Mendoza D, Altabe S (2013) Exploring the biosynthesis of unsaturated fatty acids in Bacillus cereus ATCC 14579 and functional characterization of novel acyl-lipid desaturases. Appl Environ Microbiol 79:6271–6279

    Article  PubMed  PubMed Central  Google Scholar 

  • Cvec G, Marsh D (1987) Phospholipid bilayers: physical principles and models. Wiley-Interscience, New York, pp 2–28

    Google Scholar 

  • Cybulski LE, Martin M, Mansilla MC, Fernandez A, de Mendoza D (2010) Membrane thickness cue for cold sensing in a bacterium. Curr Biol 20:1539–1544

    Article  CAS  PubMed  Google Scholar 

  • de Mendoza D (2014) Temperature sensing by membranes. Annu Rev Microbiol 68:101–116

    Article  PubMed  Google Scholar 

  • de Mendoza D, Cronan JE (1983) Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem Sci 8:49–52

    Article  Google Scholar 

  • Diomandé SE, Chamot S, Antolinos V, Vasai F, Guinebretiere MH, Bornard I, Nguyen-the C, Broussolle V (2014) The CasKR two-component system is required for the growth of mesophilic and psychrotolerant Bacillus cereus strains at low temperatures. Appl Environ Microbiol 80:2493–2503

    Article  PubMed  PubMed Central  Google Scholar 

  • Diomandé SE, Nguyen-the C, Abee T, Tempelaars MH, Broussolle V, Brillard J (2015) Involvement of the CasK/R two-component system in optimal unsaturation of the Bacillus cereus fatty acids during low-temperature growth. Int J Food Microbiol 213:110–117

    Article  PubMed  Google Scholar 

  • Diomandé SE, Doublet B, Vasaï F, Guinebretiére M-H, Broussolle V, Brillard J (2016) Expression of the genes encoding the CasK/R two-component system and the DesA desaturase during Bacillus cereus cold adaptation. FEMS Microbiol Lett 363:pii: fnw174

    Article  Google Scholar 

  • Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55:288–302

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawahara K, Tsukano H, Watanabe H, Lindner B, Matsuura M (2002) Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect Immun 70:4092–4098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein W, Weber MH, Marahiel MA (1999) Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J Bacteriol 181:5341–5349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Powell DA, Shaffer SA, Rasko DA, Pelletier MR, Leszyk JD, Scott AJ, Masoudi A, Goodlett DR, Wang X, Raetz CR, Ernst RK (2012) LPS remodeling is an evolved survival strategy for bacteria. Proc Natl Acad Sci U S A 109:8716–8721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magnuson K, Jackovski S, Rock CO, Cronan JE Jr (1993) Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol Rev 57:522–542

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mansilla MC, de Mendoza D (2005) The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Arch Microbiol 183:229–235

    Article  CAS  PubMed  Google Scholar 

  • Mansilla MC, Cybulski LE, Albanesi D, de Mendoza D (2004) Control of membrane lipid fluidity by molecular thermosensors. J Bacteriol 186:6681–6688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin M, de Mendoza D (2013) Regulation of Bacillus subtilis DesK thermosensor by lipids. Biochem J 451:269–275

    Article  CAS  PubMed  Google Scholar 

  • Martin N, Lombardia E, Altabe SG, de Mendoza D, Mansilla MC (2009) A lipA (yutB) mutant, encoding lipoic acid synthase, provides insight into the interplay between branched-chain and unsaturated fatty acid biosynthesis in Bacillus subtilis. J Bacteriol 191:7447–7455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montminy SW, Khan N, McGrath S, Walkowicz MJ, Sharp F, Conlon JE, Fukase K, Kusumoto S, Sweet C, Miyake K, Akira S, Cotter RJ, Goguen JD, Lien E (2006) Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat Immunol 7:1066–1073

    Article  CAS  PubMed  Google Scholar 

  • Parsons JB, Rock CO (2013) Bacterial lipids: metabolism and membrane homeostasis. Prog Lipid Res 52:249–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phadtare S (2004) Recent developments in bacterial cold-shock response. Curr Issues Mol Biol 6:125–136

    CAS  PubMed  Google Scholar 

  • Phetsuksiri B, Jackson M, Scherman H, McNeil M, Besra GS, Baulard AR, Slayden RA, DeBarber AE, Barry CE III, Baird MS, Crick DC, Brennan PJ (2003) Unique mechanism of action of the thiourea drug isoxyl on Mycobacterium tuberculosis. J Biol Chem 278:53123–53130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porrini L, Cybulski L, Altabe SG, Mansilla MC, de Mendoza D (2014) Cerulenin inhibits unsaturated fatty acids synthesis in Bacillus subtilis by modifying the input signal of DesK thermosensor. Microbiol Open 3:213–224

    Article  CAS  Google Scholar 

  • Raetz CR, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebeil R, Ernst RK, Jarrett CO, Adams KN, Miller SI, Hinnebusch BJ (2006) Characterization of late acyltransferase genes of Yersinia pestis and their role in temperature-dependent lipid A variation. J Bacteriol 188:1381–1388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saita E, Abriata LA, Tsai YT, Trajtenberg F, Lemmin T, Buschiazzo A, Dal Peraro M, de Mendoza D, Albanesi D (2015) A coiled coil switch mediates cold sensing by the thermosensory protein DesK. Mol Microbiol 98:258–271

    Article  CAS  PubMed  Google Scholar 

  • Saita E, Albanesi D, de Mendoza D (2016) Sensing membrane thickness: lessons learned from cold stress. Biochim Biophys Acta 1861:837–846

    Article  CAS  PubMed  Google Scholar 

  • Shimura Y, Shiraiwa Y, Suzuki I (2012) Characterization of the subdomains in the N-terminal region of histidine kinase Hik33 in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 53:1255–1266

    Article  CAS  PubMed  Google Scholar 

  • Sinetova MA, Los DA (2016) New insights in cyanobacterial cold stress responses: Genes, sensors, and molecular triggers. Biochim Biophys Acta 1860:2391–2403

    Article  CAS  PubMed  Google Scholar 

  • Singh AK, Zhang YM, Zhu K, Subramanian C, Li Z, Jayaswal RK, Gatto C, Rock CO, Wilkinson BJ (2009) FabH selectivity for anteiso branched-chain fatty acid precursors in low-temperature adaptation in Listeria monocytogenes. FEMS Microbiol Lett 301:188–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Small DM (1986) General properties of lipids conferred by the aliphatic chain. In: Hanahan DJ (ed) The physical chemistry of lipids, Handbook of lipid research, vol 4. Plenum, New York, pp 21–42

    Google Scholar 

  • Wollenweber HW, Schlecht S, Lüderitz O, Rietschel ET (1983) Fatty acid in lipopolysaccharides of Salmonella species grown at low temperature. Identification and position. Eur J Biochem 130:167–171

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y-M, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233

    Article  PubMed  Google Scholar 

  • Zhu K, Bayles DO, Xiong A, Jayaswal RK, Wilkinson BJ (2005) Precursor and temperature modulation of fatty acid composition and growth of Listeria monocytogenes cold-sensitive mutants with transposon-interrupted branched-chain-keto acid dehydrogenase. Microbiology 151:615–623

    Article  CAS  PubMed  Google Scholar 

  • Zhu K, Choi KH, Schweizer HP, Rock CO, Zhang YM (2006) Two aerobic pathways for the formation of unsaturated fatty acids in Pseudomonas aeruginosa. Mol Microbiol 60:260–273

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from Agencia Nacional de Promoción Científica y Tecnológica (FONCYT). M.C. Mansilla and D. de Mendoza are Career Investigators of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

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Authors and Affiliations

  1. Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Universidad Nacional de Rosario, Rosario, Argentina

    M. C. Mansilla

  2. Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Universidad Nacional de Rosario, Rosario, Argentina

    D. de Mendoza

Authors
  1. M. C. Mansilla
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  2. D. de Mendoza
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Correspondence to M. C. Mansilla .

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Editors and Affiliations

  1. Centro de Ciencias Genomicas, Universidad Nacional Autonoma de Mexico Centro de Ciencias Genomicas, Cuernavaca, Morelos, Mexico

    Otto Geiger

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Mansilla, M.C., de Mendoza, D. (2017). Regulation of Membrane Lipid Homeostasis in Bacteria upon Temperature Change. In: Geiger, O. (eds) Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-43676-0_56-2

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  • DOI: https://doi.org/10.1007/978-3-319-43676-0_56-2

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  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-43676-0

  • Online ISBN: 978-3-319-43676-0

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

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  1. Latest

    Regulation of Membrane Lipid Homeostasis in Bacteria upon Temperature Change
    Published:
    27 January 2017

    DOI: https://doi.org/10.1007/978-3-319-43676-0_56-2

  2. Original

    Regulation of Membrane Lipid Homeostasis in Bacteria upon Temperature Change
    Published:
    27 December 2016

    DOI: https://doi.org/10.1007/978-3-319-43676-0_56-1

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