Skip to main content
SpringerLink
Log in

Metabolic adaptability shifts of cell membrane fatty acids of Komagataeibacter hansenii HDM1-3 improve acid stress resistance and survival in acidic environments

  • Fermentation, Cell Culture and Bioengineering - Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Komagataeibacter hansenii HDM1-3 (K. hansenii HDM1-3) has been widely applied for producing bacterial cellulose (BC). The yield of BC has been frequently limited by the acidification during sugar metabolism, due to the generation of organic acids such as acetic acid. In this study, the acid resistance mechanism of K. hansenii HDM1-3 has been investigated from the aspect of metabolic adaptability of cell membrane fatty acids. Firstly, we observed that the survival rate of K. hansenii HDM1-3 was decreased with lowered pH values (adjusted with acetic acids), accompanied by increased leakage rate. Secondly, the cell membrane adaptability in response to acid stress was evaluated, including the variations of cell membrane fluidity and fatty acid composition. The proportion of unsaturated fatty acids was increased (especially, C18-1w9c and C19-Cyc), unsaturation degree and chain length of fatty acids were also increased. Thirdly, the potential molecular regulation mechanism was further elucidated. Under acid stress, the fatty acid synthesis pathway was involved in the structure and composition variations of fatty acids, which was proved by the activation of both fatty acid dehydrogenase (des) and cyclopropane fatty acid synthase (cfa) genes, as well as the addition of exogenous fatty acids. The fatty acid synthesis of K. hansenii HDM1-3 may be mediated by the activation of two-component sensor signaling pathways in response to the acid stress. The acid resistance mechanism of K. hansenii HDM1-3 adds to our knowledge of the acid stress adaptation, which may facilitate the development of new strategies for improving the industrial performance of this species under acid stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681–1691. https://doi.org/10.1093/emboj/20.7.1681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Aricha B, Fishov I, Cohen Z, Sikron N, Pesakhov S, Khozin-Goldberg I, Dagan R, Porat N (2004) Differences in membrane fluidity and fatty acid composition between phenotypic variants of Streptococcus pneumoniae. J Bacteriol 186:4638–4644. https://doi.org/10.1128/JB.186.14.4638-4644.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Asakura H, Ekawa T, Sugimoto N, Momose Y, Kawamoto K, Makino S, Igimi S, Yamamoto S (2012) Membrane topology of Salmonella invasion protein SipB confers osmotolerance. Biochem Biophys Res Commun 426:654–658. https://doi.org/10.1016/j.bbrc.2012.09.012

    Article  CAS  PubMed  Google Scholar 

  4. Badshah M, Ullah H, Khan SA, Park JK, Khan T (2017) Preparation, characterization and in vitro evaluation of bacterial cellulose matrices for oral drug delivery. Cellulose 24:5041–5052. https://doi.org/10.1007/s10570-017-1474-8

    Article  CAS  Google Scholar 

  5. Bottan S, Robotti F, Jayathissa P, Hegglin A, Bahamonde N, Heredia-Guerrero JA, Bayer IS, Scarpellini A, Merker H, Lindenblatt N, Poulikakos D, Ferrari A (2015) Surface-structured bacterial cellulose with guided assembly-based biolithography (GAB). ACS Nano 9:206–219. https://doi.org/10.1021/nn5036125

    Article  CAS  PubMed  Google Scholar 

  6. Broadbent JR, Oberg TS, Hughes JE, Ward RE, Brighton C, Welker DL, Steele JL (2014) Influence of polysorbate 80 and cyclopropane fatty acid synthase activity on lactic acid production by Lactobacillus casei ATCC 334 at low pH. J Ind Microbiol Biotechnol 41:545–553. https://doi.org/10.1007/s10295-013-1391-2

    Article  CAS  PubMed  Google Scholar 

  7. Budin-Verneuil A, Maguin E, Auffray Y, Ehrlich SD, Pichereau V (2005) Transcriptional analysis of the cyclopropane fatty acid synthase gene of Lactococcus lactis MG1363 at low pH. FEMS Microbiol Lett 250:189–194. https://doi.org/10.1016/j.femsle.2005.07.007

    Article  CAS  PubMed  Google Scholar 

  8. Chang YY, Cronan JE (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33:249–259. https://doi.org/10.1046/j.1365-2958.1999.01456.x

    Article  CAS  PubMed  Google Scholar 

  9. Chen YY, Ganzle MG (2016) Influence of cyclopropane fatty acids on heat, high pressure, acid and oxidative resistance in Escherichia coli. Int J Food Microbiol 222:16–22. https://doi.org/10.1016/j.ijfoodmicro.2016.01.017

    Article  CAS  PubMed  Google Scholar 

  10. Choi J, Groisman EA (2016) Acidic pH sensing in the bacterial cytoplasm is required for Salmonella virulence. Mol Microbiol 101:1024–1038. https://doi.org/10.1111/mmi.13439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Choi J, Groisman EA (2017) Activation of master virulence regulator PhoP in acidic pH requires the Salmonella-specific protein UgtL. Sci Signal. https://doi.org/10.1126/scisignal.aan6284

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chu-Ky S, Tourdot-Marechal R, Marechal PA, Guzzo J (2005) Combined cold, acid, ethanol shocks in Oenococcus oeni: effects on membrane fluidity and cell viability. Biochim Biophys Acta 1717:118–124. https://doi.org/10.1016/j.bbamem.2005.09.015

    Article  CAS  PubMed  Google Scholar 

  13. de la Haba C, Palacio JR, Martinez P, Morros A (2013) Effect of oxidative stress on plasma membrane fluidity of THP-1 induced macrophages. Biochim Biophys Acta 1828:357–364. https://doi.org/10.1016/j.bbamem.2012.08.013

    Article  CAS  PubMed  Google Scholar 

  14. Denich TJ, Beaudette LA, Lee H, Trevors JT (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52:149–182

    Article  CAS  Google Scholar 

  15. Diomande SE, Doublet B, Vasai F, Guinebretiere MH, 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. https://doi.org/10.1093/femsle/fnw174

    Article  PubMed  Google Scholar 

  16. Diomande 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. https://doi.org/10.1016/j.ijfoodmicro.2015.04.043

    Article  CAS  PubMed  Google Scholar 

  17. Diomande SE, Nguyen-The C, Guinebretiere MH, Broussolle V, Brillard J (2015) Role of fatty acids in Bacillus environmental adaptation. Front Microbiol 6:813. https://doi.org/10.3389/fmicb.2015.00813

    Article  PubMed  PubMed Central  Google Scholar 

  18. Fozo EM, Kajfasz JK, Quivey RG Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238:291–295. https://doi.org/10.1016/j.femsle.2004.07.047

    Article  CAS  PubMed  Google Scholar 

  19. Fozo EM, Quivey RG Jr (2004) 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 186:4152–4158. https://doi.org/10.1128/JB.186.13.4152-4158.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gautier J, Passot S, Penicaud C, Guillemin H, Cenard S, Lieben P, Fonseca F (2013) A low membrane lipid phase transition temperature is associated with a high cryotolerance of Lactobacillus delbrueckii subspecies bulgaricus CFL1. J Dairy Sci 96:5591–5602. https://doi.org/10.3168/jds.2013-6802

    Article  CAS  PubMed  Google Scholar 

  21. Guan N, Li J, Shin HD, Du G, Chen J, Liu L (2017) Microbial response to environmental stresses: from fundamental mechanisms to practical applications. Appl Microbiol Biotechnol 101:3991–4008. https://doi.org/10.1007/s00253-017-8264-y

    Article  CAS  PubMed  Google Scholar 

  22. Guo ZP, Khoomrung S, Nielsen J, Olsson L (2018) Changes in lipid metabolism convey acid tolerance in Saccharomyces cerevisiae. Biotechnol Biofuels 11:297. https://doi.org/10.1186/s13068-018-1295-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kaiser HJ, Surma MA, Mayer F, Levental I, Grzybek M, Klemm RW, Da Cruz S, Meisinger C, Muller V, Simons K, Lingwood D (2011) Molecular convergence of bacterial and eukaryotic surface order. J Biol Chem 286:40631–40637. https://doi.org/10.1074/jbc.M111.276444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kenney LJ (2018) The role of acid stress in Salmonella pathogenesis. Curr Opin Microbiol 47:45–51. https://doi.org/10.1016/j.mib.2018.11.006

    Article  CAS  PubMed  Google Scholar 

  25. Khan S, Ul-Islam M, Ikram M, Ullah MW, Israr M, Subhan F, Kim Y, Jang JH, Yoon S, Park JK (2016) Three-dimensionally microporous and highly biocompatible bacterial cellulose–gelatin composite scaffolds for tissue engineering applications. RSC Adv 6:110840–110849. https://doi.org/10.1039/c6ra18847h

    Article  CAS  Google Scholar 

  26. Kim BH, Kim S, Kim HG, Lee J, Lee IS, Park YK (2005) The formation of cyclopropane fatty acids in Salmonella enterica serovar Typhimurium. Microbiology 151:209–218. https://doi.org/10.1099/mic.0.27265-0

    Article  CAS  PubMed  Google Scholar 

  27. Lee YH, Kim JH (2017) Direct interaction between the transcription factors CadC and OmpR involved in the acid stress response of Salmonella enterica. J Microbiol 55:966–972. https://doi.org/10.1007/s12275-017-7410-7

    Article  CAS  PubMed  Google Scholar 

  28. Li L, Jia Y, Hou Q, Charles TC, Nester EW, Pan SQ (2002) A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc Natl Acad Sci USA 99:12369–12374. https://doi.org/10.1073/pnas.192439499

    Article  CAS  PubMed  Google Scholar 

  29. Li Y, Tian C, Tian H, Zhang J, He X, Ping W, Lei H (2012) Improvement of bacterial cellulose production by manipulating the metabolic pathways in which ethanol and sodium citrate involved. Appl Microbiol Biotechnol 96:1479–1487. https://doi.org/10.1007/s00253-012-4242-6

    Article  CAS  PubMed  Google Scholar 

  30. Li Y, Tian J, Tian H, Chen X, Ping W, Tian C, Lei H (2016) Mutation-based selection and analysis of Komagataeibacter hansenii HDM1-3 for improvement in bacterial cellulose production. J Appl Microbiol 121:1323–1334. https://doi.org/10.1111/jam.13244

    Article  CAS  PubMed  Google Scholar 

  31. Li YH, Lau PCY, Tang N, Svensater G, Ellen RP, Cvitkovitch DG (2002) Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J Bacteriol 184:6333–6342. https://doi.org/10.1128/jb.184.22.6333-6342.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lin Z, Cai X, Chen M, Ye L, Wu Y, Wang X, Lv Z, Shang Y, Qu D (2018) Virulence and stress responses of Shigella flexneri regulated by PhoP/PhoQ. Front Microbiol. https://doi.org/10.3389/fmicb.2017.02689

    Article  PubMed  PubMed Central  Google Scholar 

  33. Liu LP, Yang XN, Ye L, Xue DD, Liu M, Jia SR, Hou Y, Chu LQ, Zhong C (2017) Preparation and characterization of a photocatalytic antibacterial material: graphene oxide/TiO2/bacterial cellulose nanocomposite. Carbohydr Polym 174:1078–1086. https://doi.org/10.1016/j.carbpol.2017.07.042

    Article  CAS  PubMed  Google Scholar 

  34. Liu Y, Betti M, Ganzle MG (2012) High pressure inactivation of Escherichia coli, Campylobacter jejuni, and spoilage microbiota on poultry meat. J Food Prot 75:497–503. https://doi.org/10.4315/0362-028X.JFP-11-316

    Article  PubMed  Google Scholar 

  35. Liu Y, Tang H, Lin Z, Xu P (2015) Mechanisms of acid tolerance in bacteria and prospects in biotechnology and bioremediation. Biotechnol Adv 33:1484–1492. https://doi.org/10.1016/j.biotechadv.2015.06.001

    Article  CAS  PubMed  Google Scholar 

  36. Lu P, Ma D, Chen Y, Guo Y, Chen GQ, Deng H, Shi Y (2013) l-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res 23:635–644. https://doi.org/10.1038/cr.2013.13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lund P, Tramonti A, De Biase D (2014) Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev 38:1091–1125. https://doi.org/10.1111/1574-6976.12076

    Article  CAS  PubMed  Google Scholar 

  38. Mols M, van Kranenburg R, van Melis CC, Moezelaar R, Abee T (2010) Analysis of acid-stressed Bacillus cereus reveals a major oxidative response and inactivation-associated radical formation. Environ Microbiol 12:873–885. https://doi.org/10.1111/j.1462-2920.2009.02132.x

    Article  CAS  PubMed  Google Scholar 

  39. Mykytczuk NC, Trevors JT, Leduc LG, Ferroni GD (2007) Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog Biophys Mol Biol 95:60–82. https://doi.org/10.1016/j.pbiomolbio.2007.05.001

    Article  CAS  PubMed  Google Scholar 

  40. Nasution O, Lee YM, Kim E, Lee Y, Kim W, Choi W (2017) Overexpression of OLE1 enhances stress tolerance and constitutively activates the MAPK HOG pathway in Saccharomyces cerevisiae. Biotechnol Bioeng 114:620–631. https://doi.org/10.1002/bit.26093

    Article  CAS  PubMed  Google Scholar 

  41. Oyce LA, Liu P, Stebbins MJ, Hanson BC, Jarboe LR (2013) The damaging effects of short chain fatty acids on Escherichia coli membranes. Appl Microbiol Biotechnol 97(18):8317–8327

    Article  Google Scholar 

  42. Parvez S, Malik KA, Ah Kang S, Kim HY (2006) Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 100:1171–1185. https://doi.org/10.1111/j.1365-2672.2006.02963.x

    Article  CAS  PubMed  Google Scholar 

  43. Perez JC, Groisman EA (2007) Acid pH activation of the PmrA/PmrB two-component regulatory system of Salmonella enterica. Mol Microbiol 63:283–293. https://doi.org/10.1111/j.1365-2958.2006.05512.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Porrini L, Cybulski LE, 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. Microbiologyopen 3:213–224. https://doi.org/10.1002/mbo3.154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Prost LR, Daley ME, Le Sage V, Bader MW, Le Moual H, Klevit RE, Miller SI (2007) Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26:165–174. https://doi.org/10.1016/j.molcel.2007.03.008

    Article  CAS  PubMed  Google Scholar 

  46. Quivey RG Jr, Faustoferri R, Monahan K, Marquis R (2000) Shifts in membrane fatty acid profiles associated with acid adaptation of Streptococcus mutans. FEMS Microbiol Lett 189:89–92

    Article  CAS  Google Scholar 

  47. Rajwade JM, Paknikar KM, Kumbhar JV (2015) Applications of bacterial cellulose and its composites in biomedicine. Appl Microbiol Biotechnol 99:2491–2511. https://doi.org/10.1007/s00253-015-6426-3

    Article  CAS  PubMed  Google Scholar 

  48. Rodriguez-Vargas S, Sanchez-Garcia A, Martinez-Rivas JM, Prieto JA, Randez-Gil F (2007) Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. Appl Environ Microbiol 73:110–116. https://doi.org/10.1128/AEM.01360-06

    Article  CAS  PubMed  Google Scholar 

  49. Romling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–557. https://doi.org/10.1016/j.tim.2015.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ruan L, Pleitner A, Ganzle MG, McMullen LM (2011) Solute transport proteins and the outer membrane protein NmpC contribute to heat resistance of Escherichia coli AW1.7. Appl Environ Microbiol 77:2961–2967. https://doi.org/10.1128/AEM.01930-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Sandoval NR, Papoutsakis ET (2016) Engineering membrane and cell-wall programs for tolerance to toxic chemicals: beyond solo genes. Curr Opin Microbiol 33:56–66. https://doi.org/10.1016/j.mib.2016.06.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sato M, Tsuchiya H, Tani H, Yamamoto K, Yamaguchi R, Nitta H, Kanematsu N, Namikawa I, Takagi N (1991) Incorporation of fatty acids by Streptococcus mutans. FEMS Microbiol Lett 65:117–121

    Article  CAS  Google Scholar 

  53. Sheng L, Zhou X, Liu Z-Y, Wang J-w, Zhou Q, Wang L, Zhang Q, Ji S-j (2016) Changed activities of enzymes crucial to membrane lipid metabolism accompany pericarp browning in ‘Nanguo’ pears during refrigeration and subsequent shelf life at room temperature. Postharvest Biol Technol 117:1–8. https://doi.org/10.1016/j.postharvbio.2016.01.015

    Article  CAS  Google Scholar 

  54. Tabanelli G, Patrignani F, Gardini F, Vinderola G, Reinheimer J, Grazia L, Lanciotti R (2014) Effect of a sublethal high-pressure homogenization treatment on the fatty acid membrane composition of probiotic lactobacilli. Lett Appl Microbiol 58:109–117. https://doi.org/10.1111/lam.12164

    Article  CAS  PubMed  Google Scholar 

  55. Ter Beek A, Keijser BJ, Boorsma A, Zakrzewska A, Orij R, Smits GJ, Brul S (2008) Transcriptome analysis of sorbic acid-stressed Bacillus subtilis reveals a nutrient limitation response and indicates plasma membrane remodeling. J Bacteriol 190:1751–1761. https://doi.org/10.1128/JB.01516-07

    Article  CAS  PubMed  Google Scholar 

  56. Ul-Islam M, Khan S, Ullah MW, Park JK (2015) Bacterial cellulose composites: synthetic strategies and multiple applications in bio-medical and electro-conductive fields. Biotechnol J 10:1847–1861. https://doi.org/10.1002/biot.201500106

    Article  CAS  PubMed  Google Scholar 

  57. Ullah A, Orij R, Brul S, Smits GJ (2012) Quantitative analysis of the modes of growth inhibition by weak organic acids in Saccharomyces cerevisiae. Appl Environ Microbiol 78:8377–8387. https://doi.org/10.1128/AEM.02126-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Umemura T, Matsumoto Y, Ohnishi K, Homma M, Kawagishi I (2002) Sensing of cytoplasmic pH by bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices. J Biol Chem 277:1593–1598. https://doi.org/10.1074/jbc.M109930200

    Article  CAS  PubMed  Google Scholar 

  59. Velly H, Bouix M, Passot S, Penicaud C, Beinsteiner H, Ghorbal S, Lieben P, Fonseca F (2015) Cyclopropanation of unsaturated fatty acids and membrane rigidification improve the freeze-drying resistance of Lactococcus lactis subsp. lactis TOMSC161. Appl Microbiol Biotechnol 99:907–918. https://doi.org/10.1007/s00253-014-6152-2

    Article  CAS  PubMed  Google Scholar 

  60. Viarengo G, Sciara MI, Salazar MO, Kieffer PM, Furlan RL, Garcia Vescovi E (2013) Unsaturated long chain free fatty acids are input signals of the Salmonella enterica PhoP/PhoQ regulatory system. J Biol Chem 288:22346–22358. https://doi.org/10.1074/jbc.M113.472829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Weber MH, Klein W, Muller L, Niess UM, Marahiel MA (2001) Role of the Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock. Mol Microbiol 39:1321–1329

    Article  CAS  Google Scholar 

  62. Wu C, Huang J, Zhou R (2014) Progress in engineering acid stress resistance of lactic acid bacteria. Appl Microbiol Biotechnol 98:1055–1063. https://doi.org/10.1007/s00253-013-5435-3

    Article  CAS  PubMed  Google Scholar 

  63. Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol 39:1031–1039. https://doi.org/10.1007/s10295-012-1104-2

    Article  CAS  PubMed  Google Scholar 

  64. Yang XN, Xue DD, Li JY, Liu M, Jia SR, Chu LQ, Wahid F, Zhang YM, Zhong C (2016) Improvement of antimicrobial activity of graphene oxide/bacterial cellulose nanocomposites through the electrostatic modification. Carbohydr Polym 136:1152–1160. https://doi.org/10.1016/j.carbpol.2015.10.020

    Article  CAS  PubMed  Google Scholar 

  65. Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233. https://doi.org/10.1038/nrmicro1839

    Article  CAS  PubMed  Google Scholar 

  66. Zhao Y, Hindorff LA, Chuang A, Monroe-Augustus M, Lyristis M, Harrison ML, Rudolph FB, Bennett GN (2003) Expression of a cloned cyclopropane fatty acid synthase gene reduces solvent formation in Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 69:2831–2841. https://doi.org/10.1128/aem.69.5.2831-2841.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zheng DQ, Liu TZ, Chen J, Zhang K, Li O, Zhu L, Zhao YH, Wu XC, Wang PM (2013) Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Appl Microbiol Biotechnol 97:2067–2076. https://doi.org/10.1007/s00253-013-4698-z

    Article  CAS  PubMed  Google Scholar 

  68. Zschiedrich CP, Keidel V, Szurmant H (2016) Molecular mechanisms of two-component signal Transduction. J Mol Biol 428:3752–3775. https://doi.org/10.1016/j.jmb.2016.08.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported financially by the Natural Science Foundation of Heilongjiang Province (C2015023), Natural Science Foundation of Heilongjiang Province Department of Education (12541625), Heilongjiang Provincial Key Laboratory of Plant Genetic Engineering and Biological Fermentation Engineering for Cold Region, Shenzhen science and technology application demonstration project (KJYY20180201180253571) and Shenzhen science and technology key project (JSGG20171013091238230). We thank Dr. Jiliang Zhang and Dr. Senanayake Indunil Chinthani for the correction of this manuscript.

Author information

Authors and Affiliations

  1. Shenzhen Key Laboratory of Microbial Genetic Engineering, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen, 518060, People’s Republic of China

    Yuanjing Li, Bingyu Li, Yue Sun, Shuangfei Li & Ning Xie

  2. Engineering Research Center of Agricultural Microbiology Technology, Ministry of Education, Heilongjiang University, Harbin, 150500, People’s Republic of China

    Yuanjing Li, Pengfei Yan & Hong Lei

  3. College of Culture and Media, Hezhou University, Hezhou, 542800, People’s Republic of China

    Qingyun Lei

  4. Key Laboratory of Molecular Biology, College of Heilongjiang Province, School of Life Sciences, Heilongjiang University, Harbin, 150080, People’s Republic of China

    Hong Lei

Authors
  1. Yuanjing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pengfei Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qingyun Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bingyu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yue Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shuangfei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hong Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ning Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hong Lei or Ning Xie.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Yan, P., Lei, Q. et al. Metabolic adaptability shifts of cell membrane fatty acids of Komagataeibacter hansenii HDM1-3 improve acid stress resistance and survival in acidic environments. J Ind Microbiol Biotechnol 46, 1491–1503 (2019). https://doi.org/10.1007/s10295-019-02225-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10295-019-02225-y

Keywords

Search

Navigation