Applied Microbiology and Biotechnology

, Volume 101, Issue 10, pp 3991–4008 | Cite as

Microbial response to environmental stresses: from fundamental mechanisms to practical applications

  • Ningzi Guan
  • Jianghua Li
  • Hyun-dong Shin
  • Guocheng Du
  • Jian Chen
  • Long Liu


Environmental stresses are usually active during the process of microbial fermentation and have significant influence on microbial physiology. Microorganisms have developed a series of strategies to resist environmental stresses. For instance, they maintain the integrity and fluidity of cell membranes by modulating their structure and composition, and the permeability and activities of transporters are adjusted to control nutrient transport and ion exchange. Certain transcription factors are activated to enhance gene expression, and specific signal transduction pathways are induced to adapt to environmental changes. Besides, microbial cells also have well-established repair mechanisms that protect their macromolecules against damages inflicted by environmental stresses. Oxidative, hyperosmotic, thermal, acid, and organic solvent stresses are significant in microbial fermentation. In this review, we summarize the modus operandi by which these stresses act on cellular components, as well as the corresponding resistance mechanisms developed by microorganisms. Then, we discuss the applications of these stress resistance mechanisms on the production of industrially important chemicals. Finally, we prospect the application of systems biology and synthetic biology in the identification of resistant mechanisms and improvement of metabolic robustness of microorganisms in environmental stresses.


Oxidative stress Hyperosmotic stress Thermal stress Acid stress Organic solvent stress Resistance mechanism Microbial production 



This work was financially supported by the 863 project (2014AA021201), a Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, and the 111 Project (111-2-06).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Abdel-Banat BM, Hoshida H, Ano A, Nonklang S, Akada R (2010) High-temperature fermentation: how can processes for ethanol production at high temperatures become superior to the traditional process using mesophilic yeast? Appl Microbiol Biotechnol 85:861–867PubMedCrossRefGoogle Scholar
  2. Abreu-Cavalheiro A, Monteiro G (2013) Solving ethanol production problems with genetically modified yeast strains. Braz J Microbiol 44:665–671PubMedCrossRefGoogle Scholar
  3. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314:1565–1568PubMedCrossRefGoogle Scholar
  4. Amaro A, Chamorro D, Seeger M, Arredondo R, Peirano I, Jerez CA (1991) Effect of external pH perturbations on in vivo protein synthesis by the acidophilic bacterium Thiobacillus ferrooxidans. J Bacteriol 173:910–915PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ananthan J, Goldberg AL, Voellmy R (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232:522–524PubMedCrossRefGoogle Scholar
  6. Asha H (1993) Genetic and molecular characterization of osmoregulatory genes in Escherichia coli: studies of mutations in kdp Operon and Ohter K+− transport genes. Accessed 16 Apr 2014
  7. Åslund F, Zheng M, Beckwith J, Storz G (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. P Natl Acad Sci 96:6161–6165CrossRefGoogle Scholar
  8. Ballesteros I, Oliva J, Ballesteros M, Carrasco J (1993) Optimization of the simultaneous saccharification and fermentation process using thermotolerant yeasts. Appl Biochem Biotec 39:201–211CrossRefGoogle Scholar
  9. Bao Y, Jemth P, Mannervik B, Williamson G (1997) Reduction of thymine hydroperoxide by phospholipid hydroperoxide glutathione peroxidase and glutathione transferases. FEBS Lett 410:210–212PubMedCrossRefGoogle Scholar
  10. Beales N (2004) Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Compre Rev Food Sci F 3:1–20CrossRefGoogle Scholar
  11. Bleoanca I, Bahrim G (2013) Overview on brewing yeast stress factors. Rom Biotech Lett 18:8559–8572Google Scholar
  12. Bukau B (1993) Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9:671–680PubMedCrossRefGoogle Scholar
  13. Cabiscol E, Tamarit J, Ros J (2010) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8Google Scholar
  14. Çakar ZP, Seker UO, Tamerler C, Sonderegger M, Sauer U (2005) Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res 5:569–578PubMedCrossRefGoogle Scholar
  15. Carmel-Harel O, Storz G (2000) Roles of the glutathione-and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461PubMedCrossRefGoogle Scholar
  16. Caspeta L, Chen Y, Ghiaci P, Feizi A, Buskov S, Hallström BM, Petranovic D, Nielsen J (2014) Altered sterol composition renders yeast thermotolerant. Science 346:75–78PubMedCrossRefGoogle Scholar
  17. Chen YY, Gänzle MG (2016) Influence of cyclopropane fatty acids on heat, high pressure, acid and oxidative resistance in Escherichia coli. Int J Food Microbiol 222:16–22PubMedCrossRefGoogle Scholar
  18. Choi SH, Baumler DJ, Kaspar CW (2000) Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157: H7. Appl Environ Microb 66:3911–3916CrossRefGoogle Scholar
  19. Coleman ST, Fang TK, Rovinsky SA, Turano FJ, Moye-Rowley WS (2001) Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. J Biol Chem 276:244–250PubMedCrossRefGoogle Scholar
  20. Compan I, Touati D (1993) Interaction of six global transcription regulators in expression of manganese superoxide dismutase in Escherichia coli K-12. J Bacteriol 175:1687–1696PubMedPubMedCentralCrossRefGoogle Scholar
  21. Coote P, Cole M, Jones M (1991) Induction of increased thermotolerance in Saccharomyces cerevisiae may be triggered by a mechanism involving intracellular pH. J Gen Microbiol 137:1701–1708PubMedCrossRefGoogle Scholar
  22. Cornelis P, Wei Q, Andrews SC, Vinckx T (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metabolomics 3:540–579Google Scholar
  23. Cox M (1991) The RecA protein as a recombinational repair system. Mol Microbiol 5:1295–1299PubMedCrossRefGoogle Scholar
  24. De Virgilio C, Piper P, Boller T, Wiemken A (1991) Acquisition of thermotolerance in Saccharomyces cerevisiae without heat shock protein hsp104 and in the absence of protein synthesis. FEBS Lett 288:86–90PubMedCrossRefGoogle Scholar
  25. Denich T, Beaudette L, Lee H, Trevors J (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52:149–182PubMedCrossRefGoogle Scholar
  26. Denisenko O, Yarchuk O (1990) Heat shock translational control in cell-free system. Antonie Van Leeuwenhoek 58:163–168PubMedCrossRefGoogle Scholar
  27. Desmond C, Fitzgerald GF, Stanton C, Ross RP (2004) Improved stress tolerance of GroESL-overproducing Lactococcus lactis and orobiotic Lactobacillus paracasei NFBC 338. Appl Environ Microbiol 70:5929–5936PubMedPubMedCentralCrossRefGoogle Scholar
  28. Dizdaroglu M (2005) Base-excision repair of oxidative DNA damage by DNA glycosylases. Mutat Res-Fund Mol M 591:45–59CrossRefGoogle Scholar
  29. Dufourc EJ (2008) Sterols and membrane dynamics. J Chem Biol 1:63–77PubMedPubMedCentralCrossRefGoogle Scholar
  30. Edgardo A, Carolina P, Manuel R, Juanita F, Baeza J (2008) Selection of thermotolerant yeast strains Saccharomyces cerevisiae for bioethanol production. Enzyme Microb Tech 43:120–123CrossRefGoogle Scholar
  31. Esmann M, Fedosova NU, Marsh D (2008) Osmotic stress and viscous retardation of the Na, K-ATPase ion pump. Biophys J 94:2767–2776PubMedCrossRefGoogle Scholar
  32. Farizano JV, Torres MA, de las Mercedes Pescaretti M, Delgado MA (2014) The RcsCDB regulatory system plays a crucial role in the protection of Salmonella enterica serovar Typhimurium against oxidative stress. Microbiology 160:2190–2199PubMedCrossRefGoogle Scholar
  33. Foo JL, Jensen HM, Dahl RH, George K, Keasling JD, Lee TS, Leong S, Mukhopadhyay A (2014) Improving microbial biogasoline production in Escherichia coli using tolerance engineering. MBio 5:e01932–e01914PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fu RY, Bongers RS, Van Swam II, Chen J, Molenaar D, Kleerebezem M, Hugenholtz J, Li Y (2006) Introducing glutathione biosynthetic capability into Lactococcus lactis subsp. cremoris NZ9000 improves the oxidative-stress resistance of the host. Metab Eng 8:662–671PubMedCrossRefGoogle Scholar
  35. Gandhi A, Shah NP (2016) Effect of salt stress on morphology and membrane composition of Lactobacillus acidophilus, Lactobacillus casei, and Bifidobacterium bifidum, and their adhesion to human intestinal epithelial-like Caco-2 cells. J Dairy Sci 99:2594–2605PubMedCrossRefGoogle Scholar
  36. Gao L, Liu Y, Sun H, Li C, Zhao Z, Liu G (2016) Advances in mechanisms and modifications for rendering yeast thermotolerance. J Biosci Bioeng 121:599–606PubMedCrossRefGoogle Scholar
  37. Garai-Ibabe G, Saa L, Pavlov V (2013) Enzymatic product-mediated stabilization of CdS quantum dots produced in situ: application for detection of reduced glutathione, NADPH, and glutathione reductase activity. Anal Chem 85:5542–5546PubMedCrossRefGoogle Scholar
  38. García CA, Alcaraz ES, Franco MA, de Rossi BNP (2015) Iron is a signal for Stenotrophomonas maltophilia biofilm formation, oxidative stress response, OMPs expression, and virulence. Front Microbiol 6:926PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gibney PA, Schieler A, Chen JC, Rabinowitz JD, Botstein D (2015) Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter. P Natl Acad Sci 112:6116–6121CrossRefGoogle Scholar
  40. Glaasker E, Heuberger E, Konings WN, Poolman B (1998) Mechanism of osmotic activation of the quaternary ammonium compound transporter (QacT) of Lactobacillus plantarum. J Bacteriol 180:5540–5546PubMedPubMedCentralGoogle Scholar
  41. Glatz A, Pilbat A-M, Németh GL, Vince-Kontár K, Jósvay K, Hunya Á, Udvardy A, Gombos I, Péter M, Balogh G (2016) Involvement of small heat shock proteins, trehalose, and lipids in the thermal stress management in Schizosaccharomyces pombe. Cell Stress Chaperon 21:327–338CrossRefGoogle Scholar
  42. Gligorovski S, Strekowski R, Barbati S, Vione D (2015) Environmental implications of hydroxyl radicals (• OH). Chem Rev 115:13051–13092PubMedCrossRefGoogle Scholar
  43. Gottesman S, Maurizi MR (1992) Regulation by proteolysis: energy-dependent proteases and their targets. Microbiol Rev 56:592–621PubMedPubMedCentralGoogle Scholar
  44. Grant R, Filman D, Finkel S, Kolter R, Hogle J (1998) The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat Struct Mol Biol 5:294–303CrossRefGoogle Scholar
  45. Grin I, Zharkov D (2011) Eukaryotic endonuclease VIII-like proteins: new components of the base excision DNA repair system. Biochemistry-Moscow 76:80–93PubMedCrossRefGoogle Scholar
  46. Guan N, Liu L, Zhuge X, Xu Q, Li J, Du G, Chen J (2012) Genome shuffling improves acid tolerance of Propionibacterium acidipropionici and propionic acid production. Adv Chem Res 15:143–152Google Scholar
  47. Guan N, Liu L, Shin HD, Chen RR, Zhang J, Li J, Du G, Shi Z, Chen J (2013) Systems-level understanding how Propionibacterium acidipropionici respond to propionic acid stress at the microenvironment levels: mechanism and application. J Biotechnol 167:56–63PubMedCrossRefGoogle Scholar
  48. Guan N, Shin HD, Chen RR, Li J, Liu L, Du G, Chen J (2014) Understanding of how Propionibacterium acidipropionici respond to propionic acid stress at the level of proteomics. Sci Rep 4:6951PubMedPubMedCentralCrossRefGoogle Scholar
  49. Guan N, Li J, Shin HD, Wu J, Du G, Shi Z, Liu L, Chen J (2015a) Comparative metabolomics analysis of the key metabolic nodes in propionic acid synthesis in Propionibacterium acidipropionici. Metabolomics 11:1106–1116CrossRefGoogle Scholar
  50. Guan N, Zhuge X, Li J, Shin HD, Wu J, Shi Z, Liu L (2015b) Engineering propionibacteria as versatile cell factories for the production of industrially important chemicals: advances, challenges, and prospects. Appl Microbiol Biotechnol 99:585–600PubMedCrossRefGoogle Scholar
  51. Guan N, Li J, Shin HD, Du G, Chen J, Liu L (2016) Metabolic engineering of acid resistance elements to improve acid resistance and propionic acid production of Propionibacterium jensenii. Biotechnol Bioeng 113:1294–1304PubMedCrossRefGoogle Scholar
  52. van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Anton Leeuw Int J G 82:187–216CrossRefGoogle Scholar
  53. Guerzoni ME, Lanciotti R, Cocconcelli PS (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147:2255–2264PubMedCrossRefGoogle Scholar
  54. Guillot A, Obis D, Mistou MY (2000) Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int J Food Microbiol 55:47–51PubMedCrossRefGoogle Scholar
  55. Guyot S, Gervais P, Young M, Winckler P, Dumont J, Davey HM (2015) Surviving the heat: heterogeneity of response in Saccharomyces cerevisiae provides insight into thermal damage to the membrane. Environ Microbiol 17:2982–2992PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hacking A, Taylor I, Hanas C (1984) Selection of yeast able to produce ethanol from glucose at 40 °C. Appl Microbiol Biotechnol 19:361–363CrossRefGoogle Scholar
  57. Hara KY, Shimodate N, Hirokawa Y, Ito M, Baba T, Mori H, Mori H (2009) Glutathione production by efficient ATP-regenerating Escherichia coli mutants. FEMS Microbiol Lett 297:217–224PubMedCrossRefGoogle Scholar
  58. Held C, Sadowski G (2016) Compatible solutes: thermodynamic properties relevant for effective protection against osmotic stress. Fluid Phase Equilibr 407:224–235CrossRefGoogle Scholar
  59. Hemamalini R, Khare S (2014) A proteomic approach to understand the role of the outer membrane porins in the organic solvent-tolerance of Pseudomonas aeruginosa PseA. PLoS One 9:e103788PubMedPubMedCentralCrossRefGoogle Scholar
  60. Hirasawa T, Yoshikawa K, Nakakura Y, Nagahisa K, Furusawa C, Katakura Y, Shimizu H, Shioya S (2007) Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J Biotechnol 131:34–44PubMedCrossRefGoogle Scholar
  61. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol R 66:300–372CrossRefGoogle Scholar
  62. Hosseini Nezhad M, Hussain MA, Britz ML (2015) Stress responses in probiotic Lactobacillus casei. Crit Rev Food Sci 55:740–749CrossRefGoogle Scholar
  63. van Houten B, Hunter SE, Meyer JN (2016) Mitochondrial DNA damage induced autophagy, cell death, and disease. Front Biosci (Landmark Ed) 21:42–54CrossRefGoogle Scholar
  64. Huang C-S, Chang L-S, Anderson ME, Meister A (1993) Catalytic and regulatory properties of the heavy subunit of rat kidney gamma-glutamylcysteine synthetase. J Biol Chem 268:19675–19680PubMedGoogle Scholar
  65. Hubatsch I, Ridderstrom M, Mannervik B (1998) Human glutathione transferase A4-4: an alpha class enzyme with high catalytic efficiency in the conjugation of 4-hydroxynonenal and other genotoxic products of lipid peroxidation. Biochem J 330:175–179PubMedPubMedCentralCrossRefGoogle Scholar
  66. Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11:443–454PubMedPubMedCentralCrossRefGoogle Scholar
  67. Imlay JA (2015) Diagnosing oxidative stress in bacteria: not as easy as you might think. Curr Opin Microbiol 24:124–131PubMedPubMedCentralCrossRefGoogle Scholar
  68. Izawa S, Ikeda K, Miki T, Wakai Y, Inoue Y (2010) Vacuolar morphology of Saccharomyces cerevisiae during the process of wine making and Japanese sake brewing. Appl Microbiol Biotechnol 88:277–282PubMedCrossRefGoogle Scholar
  69. Jung YJ, Park HD (2005) Antisense-mediated inhibition of acid trehalase (ATH1) gene expression promotes ethanol fermentation and tolerance in Saccharomyces cerevisiae. Biotechnol Lett 27:1855–1859PubMedCrossRefGoogle Scholar
  70. Karimi K, Emtiazi G, Taherzadeh MJ (2006) Ethanol production from dilute-acid pretreated rice straw by simultaneous saccharification and fermentation with Mucor indicus, Rhizopus oryzae, and Saccharomyces cerevisiae. Enzyme Microb Tech 40:138–144CrossRefGoogle Scholar
  71. Khaskheli GB, Zuo FL, Yu R, Chen SW (2015) Overexpression of small heat shock protein enhances heat- and salt-stress tolerance of Bifidobacterium longum NCC2705. Curr Microbiol 71:8–15PubMedCrossRefGoogle Scholar
  72. Kim HS, Kim NR, Yang J, Choi W (2011) Identification of novel genes responsible for ethanol and/or thermotolerance by transposon mutagenesis in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 91:1159–1172PubMedCrossRefGoogle Scholar
  73. Kimura Y, Kawasaki S, Yoshimoto H, Takegawa K (2010) Glycine betaine biosynthesized from glycine provides an osmolyte for cell growth and spore germination during osmotic stress in Myxococcus xanthus. J Bacteriol 192:1467–1470PubMedCrossRefGoogle Scholar
  74. Koga T, Katagiri T, Hori H, Takumi K (2002) Alkaline adaptation induces cross-protection against some environmental stresses and morphological change in Vibrio parahaemolyticus. Microbiol Res 157:249–255PubMedCrossRefGoogle Scholar
  75. Krauke Y, Sychrova H (2011) Cnh1 Na+/H+ antiporter and Ena1 Na+-ATPase play different roles in cation homeostasis and cell physiology of Candida glabrata. FEMS Yeast Res 11:29–41PubMedCrossRefGoogle Scholar
  76. Kregel KC (2002) Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186PubMedCrossRefGoogle Scholar
  77. van Kuijk FJ, Sevanian A, Handelman GJ, Dratz EA (1987) A new role for phospholipase A2: protection of membranes from lipid peroxidation damage. Trends Biochem Sci 12:31–34CrossRefGoogle Scholar
  78. Li Y, Wei G, Chen J (2004) Glutathione: a review on biotechnological production. Appl Microbiol Biotechnol 66:233–242PubMedCrossRefGoogle Scholar
  79. Li Y, Hugenholtz J, Sybesma W, Abee T, Molenaar D (2005) Using Lactococcus lactis for glutathione overproduction. Appl Microbiol Biotechnol 67:83–90PubMedCrossRefGoogle Scholar
  80. Liang G, Du G, Chen J (2008a) A novel strategy of enhanced glutathione production in high cell density cultivation of Candida utilis—cysteine addition combined with dissolved oxygen controlling. Enzyme Microb Tech 42:284–289CrossRefGoogle Scholar
  81. Liang G, Du G, Chen J (2008b) Enhanced glutathione production by using low-pH stress coupled with cysteine addition in the treatment of high cell density culture of Candida utilis. Lett Appl Microbiol 46:507–512PubMedCrossRefGoogle Scholar
  82. Liang G, Liao X, Du G, Chen J (2008c) Elevated glutathione production by adding precursor amino acids coupled with ATP in high cell density cultivation of Candida utilis. J Appl Microbiol 105:1432–1440PubMedCrossRefGoogle Scholar
  83. Liang G, Liao X, Du G, Chen J (2009) A new strategy to enhance glutathione production by multiple H2O2-induced oxidative stresses in Candida utilis. Bioresour Technol 100:350–355PubMedCrossRefGoogle Scholar
  84. Liao X, Shen W, Chen J, Li Y, Du G (2006) Improved glutathione production by gene expression in Escherichia coli. Lett Appl Microbiol 43:211–214PubMedCrossRefGoogle Scholar
  85. Liao X, Deng T, Zhu Y, Du G, Chen J (2008) Enhancement of glutathione production by altering adenosine metabolism of Escherichia coli in a coupled ATP regeneration system with Saccharomyces cerevisiae. J Appl Microbiol 104:345–352PubMedCrossRefGoogle Scholar
  86. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50PubMedCrossRefGoogle Scholar
  87. Lipinska B, Zylicz M, Georgopoulos C (1990) The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase. J Bacteriol 172:1791–1797PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lipton SA, Bossy-Wetzel E (2002) Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111:147–150PubMedCrossRefGoogle Scholar
  89. Liu L, Xu O, Li Y, Shi Z, Zhu Y, Du G, Chen J (2007) Enhancement of pyruvate osmotic-tolerant mutant production by of Torulopsis glabrata. Biotechnol Bioeng 97:825–832PubMedCrossRefGoogle Scholar
  90. Liu J, Wisniewski M, Droby S, Vero S, Tian S, Hershkovitz V (2011) Glycine betaine improves oxidative stress tolerance and biocontrol efficacy of the antagonistic yeast Cystofilobasidium infirmominiatum. Int J Food Microbiol 146:76–83PubMedCrossRefGoogle Scholar
  91. Lončar N, Fraaije MW (2015) Catalases as biocatalysts in technical applications: current state and perspectives. Appl Microbiol Biotechnol 99:3351–3357PubMedCrossRefGoogle Scholar
  92. Ma R, Zhang Y, Hong H, Lu W, Lin M, Chen M, Zhang W (2011) Improved osmotic tolerance and ethanol production of ethanologenic Escherichia coli by IrrE, a global regulator of radiation-resistance of Deinococcus radiodurans. Curr Microbiol 62:659–664PubMedCrossRefGoogle Scholar
  93. Macalady J, Banfield JF (2003) Molecular geomicrobiology: genes and geochemical cycling. Earth Planet Sci Lett 209:1–17CrossRefGoogle Scholar
  94. Maeng S, Ko Y-J, Kim G-B, Jung K-W, Floyd A, Heitman J, Bahn Y-S (2010) Comparative transcriptome analysis reveals novel roles of the ras and cyclic AMP signaling pathways in environmental stress response and antifungal drug sensitivity in Cryptococcus neoformans. Eukaryot Cell 9:360–378PubMedPubMedCentralCrossRefGoogle Scholar
  95. Maiorino M, Thomas JP, Girotti AW, Ursini F (1991) Reactivity of phospholipid hydroperoxide glutathione peroxidase with membrane and lipoprotein lipid hydroperoxides. Free Radic Res Commun 12:131–135PubMedCrossRefGoogle Scholar
  96. Manuel Rodriguez-Pena J, Garcia R, Nombela C, Arroyo J (2010) The high-osmolarity glycerol (HOG) and cell wall integrity (CWI) signalling pathways interplay: a yeast dialogue between MAPK routes. Yeast 27:495–502CrossRefGoogle Scholar
  97. Marles-Wright J, Lewis RJ (2007) Stress responses of bacteria. Curr Opin Struc Biol 17:755–760CrossRefGoogle Scholar
  98. Marty-Teysset C, De La Torre F, Garel J-R (2000) Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: involvement of an NADH oxidase in oxidative stress. Appl Environ Microbiol 66:262–267PubMedPubMedCentralCrossRefGoogle Scholar
  99. Melis JP, van Steeg H, Luijten M (2013) Oxidative DNA damage and nucleotide excision repair. Antioxid Redox Sign 18:2409–2419CrossRefGoogle Scholar
  100. Metris A, George S, Mulholland F, Carter A, Baranyi J (2014) E. coli under salt stress: metabolic shift in the presence of glycine betaine. Appl Environ Microbiol 80:4745–4756PubMedPubMedCentralCrossRefGoogle Scholar
  101. Millati R, Niklasson C, Taherzadeh MJ (2002) Effect of pH, time and temperature of overliming on detoxification of dilute-acid hydrolyzates for fermentation by Saccharomyces cerevisiae. Process Biochem 38:515–522CrossRefGoogle Scholar
  102. Misra S, Sharma V, Srivastava AK (2015) Bacterial polysaccharides: an overview. In: Ramawat KG, Mérillon JM (eds) Polysaccharides: Bioactivity and Biotechnology. Springer, Switzerland, pp 81–108CrossRefGoogle Scholar
  103. Mosialou E, Ekström G, Adang AE, Morgenstern R (1993) Evidence that rat liver microsomal glutathione transferase is responsible for glutathione-dependent protection against lipid peroxidation. Biochem Pharmacol 45:1645–1651PubMedCrossRefGoogle Scholar
  104. Mukwevho E, Ferreira Z, Ayeleso A (2014) Potential role of sulfur-containing antioxidant systems in highly oxidative environments. Molecules 19:19376–19389PubMedCrossRefGoogle Scholar
  105. Nakayama H, Mitsui T, Nishihara M, Kito M (1980) Relation between growth temperature of E. coli and phase transition temperatures of its cytoplasmic and outer membranes. Biochim Biophys Acta Biomembr 601:1–10CrossRefGoogle Scholar
  106. Neves M-J, François J (1992) On the mechanism by which a heat shock induces trehalose accumulation in Saccharomyces cerevisiae. Biochem J 288:859–864PubMedPubMedCentralCrossRefGoogle Scholar
  107. Nicolaou SA, Gaida SM, Papoutsakis ET (2010) A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Metab Eng 12:307–331PubMedCrossRefGoogle Scholar
  108. Nikolouli K, Mossialos D (2016) Functional characterization of TtgABC efflux pump of the RND family in the entomopathogenic bacterium Pseudomonas entomophila. Ann Microbiol 66:499–503CrossRefGoogle Scholar
  109. Nilsen L, Forstrøm RJ, Bjørås M, Alseth IAP (2012) Endonuclease independent repair of abasic sites in Schizosaccharomyces pombe. Nucleic Acids Res 40:2000–2009PubMedCrossRefGoogle Scholar
  110. Oide S, Gunji W, Moteki Y, Yamamoto S, Suda M, Jojima T, Yukawa H, Inui M (2015) Thermal and solvent stress cross-tolerance conferred to Corynebacterium glutamicum by adaptive laboratory evolution. Appl Environ Microb 81:2284–2298CrossRefGoogle Scholar
  111. Okuda M, Niwa T, Taguchi H (2015) Single-molecule analyses of the dynamics of heat shock protein 104 (Hsp104) and protein aggregates. J Biol Chem 290:7833–7840PubMedPubMedCentralCrossRefGoogle Scholar
  112. Onraedt A, De Mey M, Walcarius B, Soetaert W, Vandamme EJ (2006) Transport kinetics of ectoine, an osmolyte produced by Brevibacterium epidermis. Biotechnol Lett 28:1741–1747PubMedCrossRefGoogle Scholar
  113. Pamplona R, Barja G, Portero-Otin M (2002) Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span. Ann N Y Acad Sci 959:475–490PubMedCrossRefGoogle Scholar
  114. Parsell D, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496PubMedCrossRefGoogle Scholar
  115. Phong TT, Hung LT, Bich Phuong LT, Hanh VT, Hoshida H, Akada R (2012) Selection and identification of thermotolerant ethanol producing yeast strains. Tap Chi Sinh Hoc 34:125–131CrossRefGoogle Scholar
  116. Piper PW (1993) Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 11:339–355PubMedCrossRefGoogle Scholar
  117. Podar M, Reysenbach AL (2006) New opportunities revealed by biotechnological explorations of extremophiles. Curr Opin Biotech 17:250–255PubMedCrossRefGoogle Scholar
  118. Price-Whelan A, Poon CK, Benson MA, Eidem TT, Roux CM, Boyd JM, Dunman PM, Torres VJ, Krulwich TA (2013) Transcriptional profiling of Staphylococcus aureus during growth in 2 M NaCl leads to clarification of physiological roles for Kdp and Ktr K+ uptake systems. MBio 4:e00407–e00413PubMedPubMedCentralCrossRefGoogle Scholar
  119. Purnick PE, Weiss R (2009) The second wave of synthetic biology: from modules to systems. Nat Rev Mol Cell Biol 10:410–422PubMedCrossRefGoogle Scholar
  120. Purvis JE, Yomano L, Ingram L (2005) Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microb 71:3761–3769CrossRefGoogle Scholar
  121. Ramos JL, Cuenca MS, Molina-Santiago C, Segura A, Duque E, Gómez-García MR, Udaondo Z, Roca A (2015) Mechanisms of solvent resistance mediated by interplay of cellular factors in Pseudomonas putida. FEMS Microbiol Rev 39:555–566PubMedCrossRefGoogle Scholar
  122. Ramotar D, Popoff SC, Gralla EB, Demple B (1991) Cellular role of yeast Apn1 apurinic endonuclease/3′-diesterase: repair of oxidative and alkylation DNA damage and control of spontaneous mutation. Mol Cell Biol 11:4537–4544PubMedPubMedCentralCrossRefGoogle Scholar
  123. Reina-Bueno M, Argandoña M, Salvador M, Rodríguez-Moya J, Iglesias-Guerra F, Csonka LN, Nieto JJ, Vargas C (2012) Role of trehalose in salinity and temperature tolerance in the model halophilic bacterium Chromohalobacter salexigens. PLoS One 7:e33587Google Scholar
  124. Russell NJ, Evans RI, terSteeg PF, Hellemons J, Verheul A, Abee T (1995) Membranes as a target for stress adaptation. Int J Food Microbiol 28:255–261PubMedCrossRefGoogle Scholar
  125. Sardessai YN (2015) Insights into organic-solvent-tolerant bacteria and their biotechnological potentials. In: Borkar S (ed) Bioprospects of coastal eubacteria. Springer International Publishing, Switzerland, pp 129–149Google Scholar
  126. Seo SW, Kim D, Szubin R, Palsson BO (2015) Genome-wide reconstruction of OxyR and SoxRS transcriptional regulatory networks under oxidative stress in Escherichia coli K-12 MG1655. Cell Rep 12:1289–1299PubMedCrossRefGoogle Scholar
  127. Sévin DC, Sauer U (2014) Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli. Nat Chem Biol 10:266–272PubMedCrossRefGoogle Scholar
  128. Shah AA, Wang C, Chung YR, Kim JY, Choi ES, Kim SW (2013) Enhancement of geraniol resistance of Escherichia coli by MarA overexpression. J Biosci Bioeng 115:253–258PubMedCrossRefGoogle Scholar
  129. Sharma P (2014) Structural and computational investigation of charge transfer mechanism in SmTGR. Master thesis No. 201061002, International Institute of Information Technology Hyderabad, IndiaGoogle Scholar
  130. Shaw AJ, Podkaminer KK, Desai SG, Bardsley JS, Rogers SR, Thorne PG, Hogsett DA, Lynd LR (2009) Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield. Int Sugar J 111:164–171Google Scholar
  131. Shi D, Wang C, Wang K (2009) Genome shuffling to improve thermotolerance, ethanol tolerance and ethanol productivity of Saccharomyces cerevisiae. J Ind Microbiol Biot 36:139–147CrossRefGoogle Scholar
  132. Shu J, Soo P, Chen J, Hsu S, Chen L, Chen C, Liang S, Buu L, Chen C (2013) Differential regulation and activity against oxidative stress of Dps proteins in Bacillus cereus. Int J Med Microbiol 303:662–673PubMedCrossRefGoogle Scholar
  133. Singer MA, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16:460–468PubMedCrossRefGoogle Scholar
  134. Stanley D, Fraser S, Chambers PJ, Rogers P, Stanley GA (2010) Generation and characterisation of stable ethanol-tolerant mutants of Saccharomyces cerevisiae. J Ind Microbiol Biot 37:139–149CrossRefGoogle Scholar
  135. Storz G (2016) New perspectives: Insights into oxidative stress from bacterial studies. Arch Biochem Biophys 595:25–27PubMedPubMedCentralCrossRefGoogle Scholar
  136. Sugimoto S, Higashi C, Matsumoto S, Sonomoto K (2010) Improvement of multiple-stress tolerance and lactic acid production in Lactococcus lactis NZ9000 under conditions of thermal stress by heterologous expression of Escherichia coli dnaK. Appl Environ Microb 76(13):4277–4285CrossRefGoogle Scholar
  137. Szczodrak J, Targoński Z (1988) Selection of thermotolerant yeast strains for simultaneous saccharification and fermentation of cellulose. Biotechnol Bioeng 31:300–303PubMedCrossRefGoogle Scholar
  138. Tao K (1999) In vivo oxidation-reduction kinetics of OxyR, the transcriptional activator for an oxidative stress-inducible regulon in Escherichia coli. FEBS Lett 457:90–92PubMedCrossRefGoogle Scholar
  139. Tarusawa T, Ito S, Goto S, Ushida C, Muto A, Himeno H (2016) (p) ppGpp-dependent and-independent pathways for salt tolerance in Escherichia coli. J Biochem. doi: 10.1093/jb/mvw008 PubMedGoogle Scholar
  140. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B (2002) Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419:174–178PubMedCrossRefGoogle Scholar
  141. Uchida K (2015) Aldehyde adducts generated during lipid peroxidation modification of proteins. Free Radic Res 49:896–904PubMedCrossRefGoogle Scholar
  142. Uyar EO, Hamamci H, Tuerkel S (2010) Effect of different stresses on trehalose levels in Rhizopus oryzae. J Basic Microbiol 50:368–372PubMedCrossRefGoogle Scholar
  143. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266:37–56PubMedCrossRefGoogle Scholar
  144. Veinger L, Diamant S, Buchner J, Goloubinoff P (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273:11032–11037PubMedCrossRefGoogle Scholar
  145. Vidal R, Lopez-Maury L, Guerrero MG, Florencio FJ (2009) Characterization of an alcohol dehydrogenase from the Cyanobacterium synechocystis sp strain PCC 6803 that responds to environmental stress conditions via the hik34-rre1 two-component system. J Biotechnol 191:4383–4391Google Scholar
  146. Wallace SS (2013) DNA glycosylases search for and remove oxidized DNA bases. Environ Mol Mutagen 54:691–704PubMedPubMedCentralCrossRefGoogle Scholar
  147. Wang T, Lu W, Lu S, Kong J (2015) Protective role of glutathione against oxidative stress in Streptococcus thermophilus. Int Dairy J 45:41–47CrossRefGoogle Scholar
  148. Warringer J, Hult M, Regot S, Posas F, Sunnerhagen P (2010) The HOG pathway dictates the short-term translational response after hyperosmotic shock. Mol Biol Cell 21:3080–3092PubMedPubMedCentralCrossRefGoogle Scholar
  149. Wei G, Li Y, Du G, Chen J (2003a) Application of a two-stage temperature control strategy for enhanced glutathione production in the batch fermentation by Candida utilis. Biotechnol Lett 25:887–890PubMedCrossRefGoogle Scholar
  150. Wei G, Li Y, Du G, Chen J (2003b) Effect of surfactants on extracellular accumulation of glutathione by Saccharomyces cerevisiae. Process Biochem 38:1133–1138CrossRefGoogle Scholar
  151. Westfall PJ, Patterson JC, Chen RE, Thorner J (2008) Stress resistance and signal fidelity independent of nuclear MAPK function. P Natl Acad Sci USA 105:12212–12217CrossRefGoogle Scholar
  152. Wiemken A (1990) Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie Van Leeuwenhoek 58:209–217PubMedCrossRefGoogle Scholar
  153. Winkler JD, Garcia C, Olson M, Callaway E, Kao KC (2014) Evolved osmotolerant Escherichia coli mutants frequently exhibit defective N-acetylglucosamine catabolism and point mutations in cell shape-regulating protein MreB. Appl Environ Microbiol 80:3729–3740PubMedPubMedCentralCrossRefGoogle Scholar
  154. Wolf A, Krämer R, Morbach S (2003) Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol Microbiol 49:1119–1134PubMedCrossRefGoogle Scholar
  155. Wong YK, Holland SI, Ertan H, Manefield M, Lee M (2016) Isolation and characterization of Dehalobacter sp. strain UNSWDHB capable of chloroform and chlorinated ethane respiration. Environ Microbiol 18:3092–3105PubMedCrossRefGoogle Scholar
  156. Wood JM (2015) Bacterial responses to osmotic challenges. J Gen Physiol 145:381–388PubMedPubMedCentralCrossRefGoogle Scholar
  157. Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biot 39:1031–1039CrossRefGoogle Scholar
  158. Wu R, Song X, Liu Q, Ma D, Xu F, Wang Q, Tang X, Wu J (2016) Gene expression of Lactobacillus plantarum FS5-5 in response to salt stress. Ann Microbiol 66:1181–1188CrossRefGoogle Scholar
  159. Wyman CE (1994) Ethanol from lignocellulosic biomass: technology, economics, and opportunities. Bioresour Technol 50:3–15CrossRefGoogle Scholar
  160. Xiong L, Teng JL, Watt RM, Kan B, Lau S, Woo P (2014) Arginine deiminase pathway is far more important than urease for acid resistance and intracellular survival in Laribacter hongkongensis: a possible result of arc gene cassette duplication. BMC Microbiol 14:42PubMedPubMedCentralCrossRefGoogle Scholar
  161. Xu S, Zhou J, Liu L, Chen J (2010) Proline enhances Torulopsis glabrata growth during hyperosmotic stress. Biotechnol Bioproc E 15:285–292CrossRefGoogle Scholar
  162. Xu S, Zhou J, Liu L, Chen J (2011) Arginine: a novel compatible solute to protect Candida glabrata against hyperosmotic stress. Process Biochem 46:1230–1235CrossRefGoogle Scholar
  163. Yaakov G, Duch A, Garcia-Rubio M, Clotet J, Jimenez J, Aguilera A, Posas F (2009) The stress-activated protein kinase Hog1 mediates S phase delay in response to osmostress. Mol Biol Cell 20:3572–3582PubMedPubMedCentralCrossRefGoogle Scholar
  164. Yazawa H, Iwahashi H, Uemura H (2007) Disruption of URA7 and GAL6 improves the ethanol tolerance and fermentation capacity of Saccharomyces cerevisiae. Yeast 24:551–560PubMedCrossRefGoogle Scholar
  165. Zaprasis A, Brill J, Thuering M, Wuensche G, Heun M, Barzantny H, Hoffmann T, Bremer E (2013) Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides. Appl Environ Microbiol 79:576–587PubMedPubMedCentralCrossRefGoogle Scholar
  166. Zhang A, Yang ST (2009) Engineering Propionibacterium acidipropionici for enhanced propionic acid tolerance and fermentation. Biotechnol Bioeng 104:766–773PubMedGoogle Scholar
  167. Zhang J, Wu C, Du G, Chen J (2012) Enhanced acid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol Bioproc E 17:283–289CrossRefGoogle Scholar
  168. Zhao X, Bai F (2009) Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production. J Biotechnol 144:23–30PubMedCrossRefGoogle Scholar
  169. Zhao Q, Zhao Y, Zhao B, Ge R, Li M, Shen Y, Huang Z (2009) Cloning and functional analysis of wheat V-H plus -ATPase subunit genes. Plant Mol Biol 69:33–46PubMedCrossRefGoogle Scholar
  170. Zhu Y, Li J, Tan M, Liu L, Li J, Sun J, Lee P, Du G, Chen J (2010) Optimization and scale-up of propionic acid production by propionic acid-tolerant Propionibacterium acidipropionici with glycerol as the carbon source. Bioresour Technol 101:8902–8906PubMedCrossRefGoogle Scholar
  171. Zhu L, Wei P, Cai J, Zhu X, Wang Z, Huang L, Xu Z (2012) Improving the productivity of propionic acid with FBB-immobilized cells of an adapted acid-tolerant Propionibacterium acidipropionici. Bioresour Technol 112:248–253PubMedCrossRefGoogle Scholar
  172. Zi Z, Liebermeister W, Klipp E (2010) A quantitative study of the Hog1 MAPK response to fluctuating osmotic stress in Saccharomyces cerevisiae. PLoS One 5:e9522PubMedPubMedCentralCrossRefGoogle Scholar
  173. Zingaro KA, Papoutsakis ET (2013) GroESL overexpression imparts Escherichia coli tolerance to i-, n-, and 2-butanol, 1, 2, 4-butanetriol and ethanol with complex and unpredictable patterns. Metab Eng 15:196–205PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Ningzi Guan
    • 1
    • 2
  • Jianghua Li
    • 1
    • 3
  • Hyun-dong Shin
    • 2
  • Guocheng Du
    • 1
    • 3
  • Jian Chen
    • 3
  • Long Liu
    • 1
    • 3
  1. 1.Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of EducationJiangnan UniversityWuxiChina
  2. 2.School of Chemical and Biomolecular EngineeringGeorgia Institute of TechnologyAtlantaUSA
  3. 3.Key Laboratory of Industrial Biotechnology, Ministry of EducationJiangnan UniversityWuxiChina

Personalised recommendations