OpenLB
Open Library of Bioscience
Advanced Search
FEMS microbiology reviews
Sep 18, 2024;48 (5):

Methods for studying microbial acid stress responses: from molecules to populations.

Merve Atasoy, Simona Bartkova, Zeynep ��etecio��lu-G��rol, Nuno P Mira, Conor O'Byrne, Fernando P��rez-Rodr��guez, Aricia Possas, Ott Scheler, Jana Sedl��kov��-Kadukov��, Mirka Sin����k, Matthias Steiger, Carmit Ziv, Peter A Lund
Author Information
  1. Merve Atasoy: UNLOCK, Wageningen University and Research, PO Box 9101, 6700 HB, the Netherlands.
  2. Simona Bartkova: Department of Chemistry and Biotechnology, Tallinn University of Technology, Ehitajate tee 5, 19086 Tallinn, Estonia.
  3. Zeynep ��etecio��lu-G��rol: Department of Industrial Biotechnology, KTH Royal Institute of Technology, Roslagstullsbacken 21 106 91 Stockholm, Stockholm, Sweden.
  4. Nuno P Mira: iBB, Institute for Bioengineering and Biosciences, Department of Bioengineering, Universidade de Lisboa, Av. Rovisco Pais, 1049-001 Lisboa, Portugal.
  5. Conor O'Byrne: Microbiology, School of Biological and Chemical Sciences, University of Galway, University Road, Galway, H91 TK33, Ireland.
  6. Fernando P��rez-Rodr��guez: Department of Food Science and Tehcnology, UIC Zoonosis y Enfermedades Emergentes ENZOEM, University of C��rdoba, 14014 C��rdoba, Spain.
  7. Aricia Possas: Department of Food Science and Tehcnology, UIC Zoonosis y Enfermedades Emergentes ENZOEM, University of C��rdoba, 14014 C��rdoba, Spain.
  8. Ott Scheler: Department of Chemistry and Biotechnology, Tallinn University of Technology, Ehitajate tee 5, 19086 Tallinn, Estonia.
  9. Jana Sedl��kov��-Kadukov��: Institute of Chemistry and Environmental Sciences, University of Ss. Cyril and Methodius, 91701 Trnava, Republic of Slovakia.
  10. Mirka Sin����k: Institute of Chemistry and Environmental Sciences, University of Ss. Cyril and Methodius, 91701 Trnava, Republic of Slovakia.
  11. Matthias Steiger: Institute of Chemical, Environmental and Bioscience Engineering, TU Wien, Getreidemarkt 9, 1060 Vienna, Austria.
  12. Carmit Ziv: Department of Postharvest Science, Agricultural Research Organization, Volcani Center, 7505101 Rishon LeZion, Israel.
  13. Peter A Lund: School of Biosciences and Institute of Microbiology of Infection, University of Birmingham, Birmingham B15 2TT, United Kingdom.
PMID: 38760882 DOI: 10.1093/femsre/fuae015

Abstract

The study of how micro-organisms detect and respond to different stresses has a long history of producing fundamental biological insights while being simultaneously of significance in many applied microbiological fields including infection, food and drink manufacture, and industrial and environmental biotechnology. This is well-illustrated by the large body of work on acid stress. Numerous different methods have been used to understand the impacts of low pH on growth and survival of micro-organisms, ranging from studies of single cells to large and heterogeneous populations, from the molecular or biophysical to the computational, and from well-understood model organisms to poorly defined and complex microbial consortia. Much is to be gained from an increased general awareness of these methods, and so the present review looks at examples of the different methods that have been used to study acid resistance, acid tolerance, and acid stress responses, and the insights they can lead to, as well as some of the problems involved in using them. We hope this will be of interest both within and well beyond the acid stress research community.

Keywords

acid resistance acid stress responses acid tolerance microbiological methods

References

  1. Appl Environ Microbiol. 2005 Nov;71(11):7033-40 [PMID: 16269739]
  2. Res Microbiol. 2023 Jun;174(5):104048 [PMID: 36893970]
  3. FEMS Microbiol Rev. 2010 Jul;34(4):554-87 [PMID: 20337722]
  4. Elife. 2020 Jan 29;9: [PMID: 31995029]
  5. J Food Prot. 2008 Sep;71(9):1835-45 [PMID: 18810867]
  6. World J Microbiol Biotechnol. 2020 May 25;36(6):81 [PMID: 32448917]
  7. Appl Environ Microbiol. 2007 May;73(10):3283-90 [PMID: 17384309]
  8. J Infect Chemother. 2000 Jun;6(2):121-5 [PMID: 11810550]
  9. Biotechnol Adv. 2020 Sep - Oct;42:107580 [PMID: 32590051]
  10. Int J Food Microbiol. 1999 Jun 1;48(3):159-66 [PMID: 10443535]
  11. BMC Microbiol. 2008 Feb 26;8:37 [PMID: 18302792]
  12. Front Microbiol. 2022 May 30;13:902110 [PMID: 35707174]
  13. J Biotechnol. 2000 Jan 28;77(1):5-15 [PMID: 10674210]
  14. Adv Biosci Biotechnol. 2011 Jun;2(3):132-137 [PMID: 21841969]
  15. Curr Biol. 2010 Jun 22;20(12):1099-103 [PMID: 20537537]
  16. Front Microbiol. 2022 Feb 15;12:822229 [PMID: 35242113]
  17. Appl Environ Microbiol. 2008 Apr;74(8):2454-60 [PMID: 18310427]
  18. J Biosci Bioeng. 2017 Feb;123(2):141-146 [PMID: 27576171]
  19. J Bacteriol. 1982 Oct;152(1):384-99 [PMID: 6749812]
  20. J Theor Biol. 2000 Jul 7;205(1):53-72 [PMID: 10860700]
  21. Biochem J. 1983 Sep 15;214(3):657-63 [PMID: 6226283]
  22. Yeast. 2021 Jul;38(7):391-400 [PMID: 34000094]
  23. Int J Food Microbiol. 2019 Sep 16;305:108254 [PMID: 31238194]
  24. IUBMB Life. 2010 Oct;62(10):715-23 [PMID: 20960531]
  25. Biotechnol Adv. 2015 Nov 15;33(7):1484-92 [PMID: 26057689]
  26. Nat Commun. 2015 Aug 10;6:7970 [PMID: 26258987]
  27. Bioinformatics. 2015 Sep 1;31(17):2882-4 [PMID: 25957349]
  28. Microorganisms. 2020 Jun 16;8(6): [PMID: 32560103]
  29. Yeast. 2004 Aug;21(11):927-46 [PMID: 15334557]
  30. Front Microbiol. 2017 Sep 29;8:1734 [PMID: 29033900]
  31. J Bacteriol. 2020 Jun 1;: [PMID: 32482722]
  32. J Biol Chem. 2019 Oct 25;294(43):15768-15780 [PMID: 31488545]
  33. J Bacteriol. 2000 Mar;182(6):1748-53 [PMID: 10692382]
  34. J Proteome Res. 2022 Dec 2;21(12):2958-2968 [PMID: 36322795]
  35. PLoS One. 2012;7(8):e43072 [PMID: 22905204]
  36. Methods. 2018 Oct 1;149:3-12 [PMID: 29715508]
  37. J Mol Biol. 2009 Oct 23;393(2):272-86 [PMID: 19703467]
  38. Food Res Int. 2018 Oct;112:353-360 [PMID: 30131146]
  39. PLoS Genet. 2017 Jul 20;13(7):e1006901 [PMID: 28727759]
  40. PLoS One. 2019 Jun 19;14(6):e0218563 [PMID: 31216328]
  41. Proteomics. 2017 Apr;17(8): [PMID: 28221718]
  42. Int J Food Microbiol. 2000 Apr 10;55(1-3):193-200 [PMID: 10791743]
  43. Sci Rep. 2020 Apr 7;10(1):6012 [PMID: 32265458]
  44. Food Res Int. 2022 Jul;157:111354 [PMID: 35761617]
  45. Microorganisms. 2020 Jul 02;8(7): [PMID: 32630740]
  46. J Antimicrob Chemother. 2012 Sep;67(9):2069-89 [PMID: 22618862]
  47. Bioessays. 2003 Mar;25(3):204-11 [PMID: 12596224]
  48. Nat Commun. 2020 Oct 23;11(1):5374 [PMID: 33097713]
  49. Dev Cell. 2020 Feb 24;52(4):461-476.e4 [PMID: 31928972]
  50. Front Microbiol. 2019 Mar 29;10:592 [PMID: 30984136]
  51. Science. 2018 Nov 9;362(6415): [PMID: 30409860]
  52. N Biotechnol. 2022 Dec 25;72:64-70 [PMID: 36150650]
  53. Bioengineering (Basel). 2016 Jan 13;3(1): [PMID: 28952569]
  54. Appl Environ Microbiol. 2018 Jan 17;84(3): [PMID: 29150517]
  55. Front Microbiol. 2019 Jan 08;9:3196 [PMID: 30671033]
  56. Int J Food Microbiol. 2022 Jan 16;361:109462 [PMID: 34749188]
  57. J Mol Biol. 2007 Oct 12;373(1):11-26 [PMID: 17765265]
  58. Int J Food Microbiol. 2008 Nov 30;128(1):51-7 [PMID: 18778863]
  59. Adv Biomed Res. 2013 Jul 30;2:75 [PMID: 24223390]
  60. Nucleic Acids Res. 2015 Feb 18;43(3):1392-406 [PMID: 25586221]
  61. J Bacteriol. 1992 Jan;174(2):530-40 [PMID: 1370290]
  62. Int J Food Microbiol. 2011 Jan 31;145(1):49-56 [PMID: 21146238]
  63. J Biosci Bioeng. 2015 Oct;120(4):396-404 [PMID: 25795572]
  64. mBio. 2022 Nov 21;13(6):e0200122 [PMID: 36409125]
  65. J Bacteriol. 1999 Apr;181(7):2209-16 [PMID: 10094700]
  66. Braz J Microbiol. 2016 Dec;47 Suppl 1:86-98 [PMID: 27825606]
  67. Front Microbiol. 2013 Nov 26;4:350 [PMID: 24324463]
  68. Res Microbiol. 2020 Oct - Nov;171(7):215-221 [PMID: 32805394]
  69. J Bacteriol. 2014 Sep;196(17):3140-9 [PMID: 24957621]
  70. J Bacteriol. 2007 Dec;189(23):8746-9 [PMID: 17905994]
  71. Front Microbiol. 2020 Apr 15;11:474 [PMID: 32351457]
  72. mBio. 2021 Aug 31;12(4):e0090921 [PMID: 34281389]
  73. FEMS Microbiol Lett. 2012 Jan;326(2):137-43 [PMID: 22092299]
  74. Nature. 1998 Jul 9;394(6689):192-5 [PMID: 9671304]
  75. Biotechnol Appl Biochem. 1993 Oct;18(2):139-42 [PMID: 8251111]
  76. J Appl Microbiol. 2018 Aug 24;: [PMID: 30144243]
  77. J Bacteriol. 2007 Aug;189(15):5601-7 [PMID: 17545292]
  78. FEMS Yeast Res. 2009 Mar;9(2):202-16 [PMID: 19220866]
  79. WormBook. 2013 Jul 09;:1-54 [PMID: 23908055]
  80. G3 (Bethesda). 2015 Jan 29;5(4):497-505 [PMID: 25636313]
  81. Appl Environ Microbiol. 2015 Mar;81(6):1932-41 [PMID: 25556191]
  82. PLoS One. 2015 Aug 18;10(8):e0135868 [PMID: 26285202]
  83. Microlife. 2022 Sep 21;3:uqac020 [PMID: 37223351]
  84. Genome Biol. 2012 Sep 10;13(9):R80 [PMID: 23021432]
  85. Int J Food Microbiol. 2019 Feb 16;291:181-188 [PMID: 30530095]
  86. Sci Rep. 2018 Aug 10;8(1):11985 [PMID: 30097598]
  87. Front Microbiol. 2021 Sep 20;12:691248 [PMID: 34616373]
  88. Front Microbiol. 2018 Feb 21;9:274 [PMID: 29515554]
  89. Food Microbiol. 2015 Feb;45(Pt B):266-75 [PMID: 25500392]
  90. Microbiol Rev. 1996 Dec;60(4):641-96 [PMID: 8987359]
  91. Arch Microbiol. 2013 May;195(5):339-48 [PMID: 23455450]
  92. Nat Microbiol. 2023 Oct;8(10):1846-1862 [PMID: 37653008]
  93. Water Res. 2019 Mar 15;151:110-133 [PMID: 30594081]
  94. Biochemistry. 2021 Nov 23;60(46):3436-3440 [PMID: 33939915]
  95. Int J Food Microbiol. 2005 Apr 15;100(1-3):231-7 [PMID: 15854708]
  96. Appl Environ Microbiol. 2012 Apr;78(7):2213-20 [PMID: 22287000]
  97. Int J Food Microbiol. 2018 Dec 20;287:18-27 [PMID: 29032838]
  98. J Bacteriol. 2010 May;192(9):2445-58 [PMID: 20207759]
  99. Front Microbiol. 2019 Jan 30;10:60 [PMID: 30761108]
  100. Genome Biol. 2009;10(5):R47 [PMID: 19409083]
  101. FEMS Microbiol Ecol. 2013 Apr;84(1):213-22 [PMID: 23228034]
  102. Front Microbiol. 2017 Jun 13;8:1009 [PMID: 28659871]
  103. Appl Environ Microbiol. 1981 May;41(5):1254-61 [PMID: 16345777]
  104. Microb Biotechnol. 2019 Jul;12(4):799-813 [PMID: 31162835]
  105. Yeast. 2014 Jun;31(6):219-32 [PMID: 24691985]
  106. Appl Microbiol Biotechnol. 2020 Apr;104(7):3097-3107 [PMID: 32047990]
  107. Foodborne Pathog Dis. 2013 Feb;10(2):107-19 [PMID: 23441912]
  108. J Bacteriol. 1994 Apr;176(8):2252-8 [PMID: 8157593]
  109. Annu Rev Microbiol. 2010;64:357-72 [PMID: 20528688]
  110. Appl Environ Microbiol. 1999 Jul;65(7):3048-55 [PMID: 10388702]
  111. Microorganisms. 2020 Sep 04;8(9): [PMID: 32899650]
  112. Front Microbiol. 2020 Jun 03;11:1078 [PMID: 32582066]
  113. Analyst. 2023 Sep 11;148(18):4242-4262 [PMID: 37581493]
  114. J Food Prot. 1992 Dec;55(12):973-979 [PMID: 31084096]
  115. mSphere. 2016 Aug 24;1(4): [PMID: 27579369]
  116. ISME J. 2013 Dec;7(12):2400-10 [PMID: 23887172]
  117. Nat Rev Microbiol. 2011 May;9(5):330-43 [PMID: 21464825]
  118. Microbiology (Reading). 2019 Jun;165(6):593-610 [PMID: 30843781]
  119. FEMS Microbiol Rev. 2010 Jul;34(4):415-25 [PMID: 20059548]
  120. Microbiology (Reading). 2007 Jan;153(Pt 1):247-53 [PMID: 17185553]
  121. Foodborne Pathog Dis. 2012 Apr;9(4):331-7 [PMID: 22356573]
  122. PLoS Pathog. 2017 Nov 9;13(11):e1006621 [PMID: 29121119]
  123. J Appl Microbiol. 2003;94(4):555-60 [PMID: 12631190]
  124. Methods Mol Biol. 2014;1157:233-47 [PMID: 24792563]
  125. BMC Syst Biol. 2017 Jan 6;11(1):1 [PMID: 28061857]
  126. Appl Environ Microbiol. 2005 May;71(5):2501-10 [PMID: 15870340]
  127. Nat Biotechnol. 2022 Jul;40(7):1132-1142 [PMID: 35468954]
  128. Int J Food Microbiol. 2009 Aug 31;134(1-2):57-62 [PMID: 19171404]
  129. G3 (Bethesda). 2017 Jan 5;7(1):1-18 [PMID: 27815348]
  130. Mol Syst Biol. 2020 Jun;16(6):e9478 [PMID: 32500952]
  131. Microbiology (Reading). 2009 Jan;155(Pt 1):268-278 [PMID: 19118367]
  132. Methods Mol Biol. 2021;2234:147-155 [PMID: 33165787]
  133. FEMS Microbiol Rev. 2022 Nov 2;46(6): [PMID: 36001464]
  134. Food Microbiol. 2021 Apr;94:103657 [PMID: 33279082]
  135. J Phycol. 2018 Oct;54(5):720-733 [PMID: 30055054]
  136. FEMS Microbiol Rev. 2022 Nov 2;46(6): [PMID: 35906711]
  137. J Mol Biol. 2010 Sep 3;401(5):726-42 [PMID: 20603130]
  138. Front Microbiol. 2022 May 26;13:829719 [PMID: 35722283]
  139. Nat Rev Microbiol. 2004 Nov;2(11):898-907 [PMID: 15494746]
  140. Appl Environ Microbiol. 1999 Aug;65(8):3681-9 [PMID: 10427066]
  141. Microb Ecol. 1982 Dec;8(4):313-23 [PMID: 24226049]
  142. Appl Environ Microbiol. 2017 May 31;83(12): [PMID: 28389540]
  143. Proteomics. 2005 Dec;5(18):4794-807 [PMID: 16237734]
  144. J Bacteriol. 2024 Apr 18;206(4):e0006924 [PMID: 38488356]
  145. PLoS One. 2020 Jun 18;15(6):e0234849 [PMID: 32555627]
  146. Curr Opin Biotechnol. 2020 Jun;63:54-62 [PMID: 31891864]
  147. Anal Chem. 2019 Jul 2;91(13):8466-8475 [PMID: 31247720]
  148. Appl Environ Microbiol. 2005 Jun;71(6):2902-9 [PMID: 15932984]
  149. Foods. 2021 Feb 07;10(2): [PMID: 33562291]
  150. FEMS Yeast Res. 2006 Sep;6(6):924-36 [PMID: 16911514]
  151. PLoS One. 2015 May 11;10(5):e0126210 [PMID: 25961572]
  152. Appl Microbiol Biotechnol. 2010 Oct;88(3):605-20 [PMID: 20697707]
  153. Res Microbiol. 2016 Sep;167(7):529-38 [PMID: 27394987]
  154. Front Microbiol. 2023 Mar 15;14:1149903 [PMID: 37007468]
  155. Microb Cell Fact. 2013 Jul 01;12:64 [PMID: 23815749]
  156. Microb Cell Fact. 2016 Oct 13;15(1):176 [PMID: 27737709]
  157. Front Microbiol. 2020 Sep 24;11:556140 [PMID: 33117305]
  158. Food Microbiol. 2015 Feb;45(Pt A):111-8 [PMID: 25481067]
  159. J Sci Food Agric. 2021 May;101(7):2892-2900 [PMID: 33159330]
  160. BMC Genomics. 2016 May 04;17:330 [PMID: 27146851]
  161. Int J Food Microbiol. 2019 Feb 2;290:226-236 [PMID: 30368088]
  162. Microbiol Mol Biol Rev. 2018 Jul 25;82(3): [PMID: 30045954]
  163. Gene. 1996;173(1 Spec No):33-8 [PMID: 8707053]
  164. J Environ Sci (China). 2023 May;127:441-452 [PMID: 36522076]
  165. J Bacteriol. 2018 Jun 25;200(14): [PMID: 29735759]
  166. Front Microbiol. 2021 Oct 01;12:711893 [PMID: 34659141]
  167. Int J Mol Sci. 2021 Jul 15;22(14): [PMID: 34299216]
  168. J Bacteriol. 2012 Jan;194(2):303-6 [PMID: 22081388]
  169. Food Microbiol. 2020 Jun;88:103399 [PMID: 31997756]
  170. Appl Environ Microbiol. 2005 Mar;71(3):1515-21 [PMID: 15746355]
  171. Mol Microbiol. 2014 Sep;93(5):911-27 [PMID: 24995530]
  172. Extremophiles. 2013 Nov;17(6):911-20 [PMID: 23974983]
  173. Foods. 2020 Jan 24;9(2): [PMID: 31991695]
  174. FEBS Lett. 2009 Dec 17;583(24):3966-73 [PMID: 19850042]
  175. Int J Food Microbiol. 2004 Jan 15;90(2):171-9 [PMID: 14698098]
  176. Front Microbiol. 2016 Oct 25;7:1672 [PMID: 27826291]
  177. Nat Rev Microbiol. 2010 Jan;8(1):15-25 [PMID: 19946288]
  178. Commun Biol. 2022 Apr 7;5(1):327 [PMID: 35393532]
  179. Food Microbiol. 2013 Dec;36(2):440-6 [PMID: 24010627]
  180. Trends Genet. 2003 Apr;19(4):224-31 [PMID: 12683976]
  181. Microbiol Res. 2009;164(6):613-23 [PMID: 17993268]
  182. Sci Rep. 2021 Jun 16;11(1):12652 [PMID: 34135398]
  183. Environ Microbiol. 2008 Jan;10(1):228-37 [PMID: 17894815]
  184. Microbiome. 2017 Aug 16;5(1):86 [PMID: 28810907]
  185. Mol Biol Cell. 2004 Feb;15(2):706-20 [PMID: 14617816]
  186. ISME J. 2015 Jun;9(6):1280-94 [PMID: 25361395]
  187. Int J Food Microbiol. 2016 Dec 5;238:241-251 [PMID: 27681379]
  188. BMC Microbiol. 2014 Jan 02;14:3 [PMID: 24383402]
  189. Appl Environ Microbiol. 2012 May;78(10):3706-14 [PMID: 22427503]
  190. Front Microbiol. 2019 Oct 29;10:2455 [PMID: 31736901]
  191. Biochem J. 1942 Sep;36(7-9):600-18 [PMID: 16747564]
  192. Compr Rev Food Sci Food Saf. 2004 Jan;3(1):1-20 [PMID: 33430556]
  193. Science. 2010 Aug 27;329(5995):1085-8 [PMID: 20798321]
  194. Int J Food Microbiol. 2008 Nov 30;128(1):136-45 [PMID: 18675486]
  195. Genes (Basel). 2020 Jun 16;11(6): [PMID: 32560106]
  196. Microbiol Spectr. 2023 Feb 14;11(1):e0275022 [PMID: 36541787]
  197. Curr Opin Microbiol. 2015 Jun;25:97-102 [PMID: 26048196]
  198. Microbiol Mol Biol Rev. 2020 Jan 15;84(1): [PMID: 31941768]
  199. Appl Environ Microbiol. 2009 Feb;75(4):981-90 [PMID: 19114526]
  200. Nat Nanotechnol. 2009 May;4(5):325-30 [PMID: 19421220]
  201. BMC Genomics. 2010 Jun 24;11:404 [PMID: 20576116]
  202. FEBS J. 2022 Apr;289(7):1723-1730 [PMID: 33751796]
  203. Front Microbiol. 2020 Apr 24;11:535 [PMID: 32390952]
  204. Cell Syst. 2017 Apr 26;4(4):393-403.e5 [PMID: 28342718]
  205. Science. 2014 Jan 10;343(6167):204-8 [PMID: 24408438]
  206. J Biol Chem. 2019 Aug 2;294(31):11685-11700 [PMID: 31197038]
  207. Nat Rev Microbiol. 2022 Nov;20(11):657-670 [PMID: 35641670]
  208. Curr Microbiol. 2001 Jan;42(1):21-5 [PMID: 11116392]
  209. Appl Microbiol Biotechnol. 2021 Jan;105(2):725-739 [PMID: 33386897]
  210. Mol Microbiol. 1996 Sep;21(5):925-40 [PMID: 8885264]
  211. J Gen Physiol. 1970 Jun;55(6):758-86 [PMID: 5424377]
  212. PLoS Comput Biol. 2017 Sep 18;13(9):e1005731 [PMID: 28922354]
  213. J Bacteriol. 1922 Mar;7(2):239-56 [PMID: 16558952]
  214. Genes (Basel). 2020 Nov 11;11(11): [PMID: 33187233]
  215. Int J Food Microbiol. 2007 Dec 15;120(3):237-49 [PMID: 17961778]
  216. Mol Biol Evol. 2003 May;20(5):686-93 [PMID: 12679550]
  217. Res Microbiol. 2023 Jun;174(5):104061 [PMID: 37055003]
  218. mBio. 2019 Sep 17;10(5): [PMID: 31530676]
  219. Biotechnol Biofuels. 2016 Nov 9;9:240 [PMID: 27843489]
  220. Evol Bioinform Online. 2016 May 12;12(Suppl 1):5-16 [PMID: 27199545]
  221. J Food Prot. 2010 Jan;73(1):140-202 [PMID: 20051217]
  222. Foods. 2021 Sep 08;10(9): [PMID: 34574229]
  223. Microbiol Mol Biol Rev. 2012 Sep;76(3):597-625 [PMID: 22933562]
  224. J Hyg (Lond). 1962 Jun;60:193-207 [PMID: 14451045]
  225. Mol Microbiol. 1989 May;3(5):609-20 [PMID: 2527331]
  226. Chem Rev. 2013 Apr 10;113(4):2437-68 [PMID: 23506082]
  227. ISME J. 2013 Oct;7(10):2034-43 [PMID: 23677010]
  228. Nat Commun. 2017 Nov 14;8(1):1587 [PMID: 29138484]
  229. Microbiol Rev. 1985 Dec;49(4):359-78 [PMID: 3912654]
  230. Genes (Basel). 2020 Dec 31;12(1): [PMID: 33396416]
  231. Genes Cells. 1998 Apr;3(4):203-8 [PMID: 9663655]
  232. Curr Opin Microbiol. 2015 Feb;23:133-40 [PMID: 25483350]
  233. J Bacteriol. 1940 Apr;39(4):389-97 [PMID: 16560300]
  234. Microbiology (Reading). 1996 Oct;142 ( Pt 10):2975-82 [PMID: 8885415]
  235. Nat Rev Microbiol. 2021 Dec;19(12):774-785 [PMID: 34183820]
  236. Fungal Genet Biol. 2013 Sep-Oct;58-59:116-25 [PMID: 23994320]
  237. FEMS Microbiol Rev. 2014 Nov;38(6):1091-125 [PMID: 24898062]
  238. iScience. 2022 Feb 11;25(4):103907 [PMID: 35340431]
  239. Appl Environ Microbiol. 1982 Jan;43(1):97-103 [PMID: 7034648]
  240. mSystems. 2021 Aug 31;6(4):e0041821 [PMID: 34313457]
  241. J Microbiol Methods. 2015 Dec;119:196-202 [PMID: 26541062]
  242. Mol Microbiol. 1995 Jul;17(1):155-67 [PMID: 7476202]
  243. Int J Food Microbiol. 2011 Mar 1;145 Suppl 1:S96-102 [PMID: 20951457]
  244. Int J Food Microbiol. 2023 Jun 2;394:110165 [PMID: 36933360]
  245. J Bacteriol. 2020 Apr 9;202(9): [PMID: 32094160]
  246. Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6241-6 [PMID: 22454494]
  247. Mol Syst Biol. 2011 Jul 05;7:509 [PMID: 21734648]
  248. Front Microbiol. 2018 Dec 11;9:3038 [PMID: 30619129]
  249. Appl Environ Microbiol. 2022 May 24;88(10):e0005122 [PMID: 35481758]
  250. Microbiol Spectr. 2021 Dec 22;9(3):e0015521 [PMID: 34878334]
  251. J Bacteriol. 1998 Jul;180(14):3650-6 [PMID: 9658010]
  252. Microb Biotechnol. 2012 Jul;5(4):509-22 [PMID: 22221537]
  253. Mol Plant Pathol. 2007 Sep;8(5):611-22 [PMID: 20507525]
  254. Front Microbiol. 2018 Mar 23;9:535 [PMID: 29662477]
  255. J Proteome Res. 2011 Oct 7;10(10):4579-96 [PMID: 21879708]
  256. Curr Opin Biotechnol. 2023 Feb;79:102885 [PMID: 36641904]
  257. J Proteome Res. 2012 Apr 6;11(4):2409-26 [PMID: 22372944]
  258. FEBS Lett. 1982 Mar 8;139(1):121-4 [PMID: 7042384]
  259. Annu Rev Microbiol. 1985;39:219-42 [PMID: 2998266]
  260. Microbiology (Reading). 2016 Aug;162(8):1422-1434 [PMID: 27230583]
  261. Mol Microbiol. 1996 Oct;22(2):367-78 [PMID: 8930920]
  262. Microb Cell Fact. 2010 Oct 25;9:79 [PMID: 20973990]
  263. Front Microbiol. 2013 Jun 18;4:157 [PMID: 23785365]
  264. Genes (Basel). 2021 Mar 25;12(4): [PMID: 33806186]
  265. Microbiology (Reading). 2009 Oct;155(Pt 10):3322-3332 [PMID: 19608608]
  266. BMC Genomics. 2019 May 9;20(1):358 [PMID: 31072330]
  267. J Appl Microbiol. 2004;96(2):359-66 [PMID: 14723697]
  268. Nat Commun. 2018 Dec 17;9(1):5333 [PMID: 30559445]
  269. J Bacteriol. 1992 Apr;174(8):2659-69 [PMID: 1556085]
  270. Annu Rev Genet. 2018 Nov 23;52:321-348 [PMID: 30476446]
  271. Nat Commun. 2018 Oct 17;9(1):4306 [PMID: 30333483]
  272. Electrophoresis. 1999 Aug;20(11):2214-24 [PMID: 10493126]
  273. Biotechnol Bioeng. 1990 May;35(11):1102-10 [PMID: 18592488]
  274. Curr Opin Microbiol. 2018 Jun;43:186-192 [PMID: 29494845]
  275. OMICS. 2010 Oct;14(5):525-40 [PMID: 20955006]
  276. Nat Rev Genet. 2020 Sep;21(9):526-540 [PMID: 32533119]
  277. Extremophiles. 2020 Mar;24(2):329-337 [PMID: 31980944]
  278. J Microbiol Methods. 2013 Mar;92(3):381-6 [PMID: 23318550]
  279. Food Microbiol. 2016 Oct;59:196-204 [PMID: 27375260]
  280. Sci Adv. 2023 Apr 28;9(17):eadf8998 [PMID: 37115929]
  281. Adv Microb Physiol. 2009;55:1-79, 317 [PMID: 19573695]
  282. J Bacteriol. 1994 Mar;176(5):1422-6 [PMID: 8113183]
  283. J Fungi (Basel). 2022 Apr 20;8(5): [PMID: 35628675]
  284. J Bacteriol. 1987 Jul;169(7):3001-6 [PMID: 2954947]
  285. Sci Rep. 2018 Oct 31;8(1):16105 [PMID: 30382109]
  286. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6271-5 [PMID: 7031646]
  287. Appl Environ Microbiol. 2019 Jul 1;85(14): [PMID: 31076436]
  288. Nat Rev Genet. 2017 Jan;18(1):41-50 [PMID: 27840430]
  289. Ecotoxicol Environ Saf. 2022 May 1;236:113499 [PMID: 35405525]
  290. Environ Pollut. 2021 Jan 1;268(Pt B):115709 [PMID: 33010675]
  291. J Immunol Methods. 2000 Sep 21;243(1-2):191-210 [PMID: 10986415]
  292. Mycologia. 2016 Nov/Dec;108(6):1049-1068 [PMID: 27760854]
  293. Extremophiles. 2013 Jul;17(4):689-96 [PMID: 23712908]
  294. ISME J. 2015 Jul;9(7):1579-92 [PMID: 25535937]
  295. Biochemistry. 1966 Feb;5(2):467-77 [PMID: 5942950]
  296. J Biosci Bioeng. 2022 Dec;134(6):521-527 [PMID: 36207257]
  297. Environ Microbiol. 2017 Jan;19(1):361-380 [PMID: 27883255]
  298. Microbiol Mol Biol Rev. 2020 Nov 11;84(4): [PMID: 33177189]
  299. Nat Biotechnol. 2013 Sep;31(9):814-21 [PMID: 23975157]
  300. Philos Trans R Soc Lond B Biol Sci. 2020 May 11;375(1798):20190256 [PMID: 32200743]
  301. Environ Microbiol. 2008 Apr;10(4):836-50 [PMID: 18248453]
  302. PLoS One. 2013 Oct 29;8(10):e77600 [PMID: 24204887]
  303. J Ind Microbiol Biotechnol. 2019 Dec;46(12):1643-1656 [PMID: 31420797]
  304. Methods Mol Biol. 2018;1730:345-357 [PMID: 29363087]
  305. PLoS Pathog. 2022 Mar 11;18(3):e1010213 [PMID: 35275969]
  306. Protein Expr Purif. 1996 Dec;8(4):430-8 [PMID: 8954890]
  307. Appl Environ Microbiol. 2009 Jul;75(13):4599-615 [PMID: 19429552]
  308. Proc Natl Acad Sci U S A. 2020 Nov 10;117(45):27954-27961 [PMID: 33106428]
  309. Food Microbiol. 2015 Feb;45(Pt B):290-9 [PMID: 25500394]
  310. Appl Microbiol Biotechnol. 2020 Jan;104(1):51-65 [PMID: 31773206]
  311. Microbiology (Reading). 2007 Jul;153(Pt 7):2289-2303 [PMID: 17600073]
  312. Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4631-6 [PMID: 15070769]
  313. Appl Environ Microbiol. 2008 Nov;74(22):6848-58 [PMID: 18806006]
  314. Front Microbiol. 2023 Mar 21;14:1131000 [PMID: 37025640]
  315. J Food Prot. 2012 Dec;75(12):2142-50 [PMID: 23212010]
  316. Curr Opin Biotechnol. 2018 Feb;49:148-155 [PMID: 28869826]
  317. Metabolites. 2013 Dec 30;4(1):1-35 [PMID: 24958385]
  318. Nat Commun. 2019 May 13;10(1):2128 [PMID: 31086182]
  319. Appl Environ Microbiol. 2006 Nov;72(11):7168-75 [PMID: 16980434]
  320. Trends Microbiol. 2008 Jun;16(6):291-300 [PMID: 18457952]
  321. Front Microbiol. 2018 Nov 15;9:2869 [PMID: 30498489]
  322. PLoS One. 2012;7(10):e47035 [PMID: 23071704]
  323. Microbiol Mol Biol Rev. 2020 Oct 28;84(4): [PMID: 33115939]
  324. Microbiology (Reading). 2020 Feb;166(2):141-148 [PMID: 31625833]
  325. Appl Environ Microbiol. 2000 Jun;66(6):2330-5 [PMID: 10831407]
  326. Int J Syst Evol Microbiol. 2019 Sep;69(9):2907-2913 [PMID: 31274405]
  327. Anal Biochem. 1986 Jul;156(1):202-12 [PMID: 3740410]
  328. Curr Opin Microbiol. 2015 Jun;25:17-24 [PMID: 25835153]
  329. PLoS Genet. 2013 Jun;9(6):e1003576 [PMID: 23818867]
  330. Front Microbiol. 2018 Nov 22;9:2656 [PMID: 30524381]
  331. Appl Environ Microbiol. 2015 Nov;81(22):7813-21 [PMID: 26341199]
  332. PLoS Biol. 2015 Apr 14;13(4):e1002116 [PMID: 25875623]
  333. Curr Microbiol. 2020 Nov;77(11):3724-3730 [PMID: 32945904]
  334. PLoS One. 2020 Sep 23;15(9):e0233872 [PMID: 32966309]
  335. mBio. 2015 Apr 14;6(2): [PMID: 25873380]
  336. Biochim Biophys Acta. 1981 Dec;650(2-3):151-66 [PMID: 6277371]
  337. Sci Rep. 2016 Jul 11;6:29278 [PMID: 27404346]
  338. Can J Microbiol. 2012 Sep;58(9):1112-23 [PMID: 22913877]
  339. Food Microbiol. 2009 Sep;26(6):592-7 [PMID: 19527834]
  340. Curr Opin Microbiol. 2018 Jun;43:139-147 [PMID: 29414445]
  341. Genet Res. 1965 Feb;6:13-26 [PMID: 14301537]
  342. FEMS Microbiol Lett. 2003 Apr 11;221(1):25-30 [PMID: 12694906]
  343. Appl Environ Microbiol. 1995 Apr;61(4):1669-72 [PMID: 7747983]
  344. J Bacteriol. 2002 Dec;184(23):6551-8 [PMID: 12426343]
  345. Appl Environ Microbiol. 1998 Feb;64(2):779-83 [PMID: 9464423]
  346. J Bacteriol. 1980 Dec;144(3):952-6 [PMID: 7002915]
  347. J Food Prot. 2001 Dec;64(12):1922-8 [PMID: 11770618]
  348. Arch Microbiol. 2015 Aug;197(6):833-41 [PMID: 25990453]
  349. Microbiol Spectr. 2022 Dec 21;10(6):e0375722 [PMID: 36453903]
  350. Microbiology (Reading). 1999 Jul;145 ( Pt 7):1703-1709 [PMID: 10439409]
  351. FEMS Microbiol Lett. 2016 May;363(10): [PMID: 27036143]
  352. Nat Commun. 2022 Jul 21;13(1):4215 [PMID: 35864107]
  353. J Environ Manage. 2022 Oct 1;319:115700 [PMID: 35982552]
  354. Front Microbiol. 2018 Apr 30;9:846 [PMID: 29760688]
  355. J Biotechnol. 2013 Aug 10;167(1):56-63 [PMID: 23792099]
  356. Appl Environ Microbiol. 1996 Jan;62(1):178-83 [PMID: 16535209]
  357. J Bacteriol. 1994 Mar;176(6):1729-37 [PMID: 8132468]
  358. Appl Environ Microbiol. 2016 Oct 14;82(21):6463-6471 [PMID: 27565617]
  359. Chemosphere. 2003 Apr;51(1):47-54 [PMID: 12586155]
  360. Int J Food Microbiol. 1997 Apr 1;35(2):103-7 [PMID: 9105917]

Grants

  1. CA18113/COST

MeSH Term

Acids
Stress, Physiological
Bacteria
Hydrogen-Ion Concentration
Bacterial Physiological Phenomena

Chemicals

Acids
Journal Article Review
Article has an altmetric score of 1

Word Cloud

Created with Highcharts 10.0.0acidstressmethodsdifferentstudymicro-organismsinsightsmicrobiologicallargeusedpopulationsmicrobialresistancetoleranceresponseswelldetectrespondstresseslonghistoryproducingfundamentalbiologicalsimultaneouslysignificancemanyappliedfieldsincludinginfectionfooddrinkmanufactureindustrialenvironmentalbiotechnologywell-illustratedbodyworkNumerousunderstandimpactslowpHgrowthsurvivalrangingstudiessinglecellsheterogeneousmolecularbiophysicalcomputationalwell-understoodmodelorganismspoorlydefinedcomplexconsortiaMuchgainedincreasedgeneralawarenesspresentreviewlooksexamplescanleadproblemsinvolvedusinghopewillinterestwithinbeyondresearchcommunityMethodsstudyingresponses:molecules

Similar Articles

Cited By