Microbial stress priming: A meta-analysis

Environmental Microbiology

Volumn 18, Issue 4, 2016, Pages 1277-1288

  Andrade Linares, Diana R ^a,b   Lehmann, Anika ^a,b   Rillig, Matthias C ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b BERLIN BRANDENBURG INSTITUTE OF ADVANCED BIODIVERSITY RESEARCH BBIB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; FUNGUS; META ANALYSIS; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGY; TEMPERATURE;

ADAPTATION, PHYSIOLOGICAL; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; FUNGI; OSMOTIC PRESSURE; TEMPERATURE;

EID: 84963621584     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13223     Document Type: Article

References (65)

1. Acar, M., Becskei, A., and van Oudenaarden, A. (2005) Enhancement of cellular memory by reducing stochastic transitions. Nature 435: 228-232.
2. Acar, M., Mettetal, J.T., and Oudenaarden, A. (2008) Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40: 471-475.
3. Adams, D.C., Gurevitch, J., and Rosenberg, M.S. (1997) Resampling tests for meta-analysis of ecological data. Ecology 78: 1277-1283.
4. Begley, M., Gahan, C.G.M., and Hill, C. (2002) Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl Environ Microbiol 68: 6005-6012.
5. Berry, D.B., and Gasch, A.P. (2008) Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol Biol Cell 19: 4580-4587.
6. Berry, D.B., Guan, Q., Hose, J., Haroon, S., Gebbia, M., Heisler, L.E., etal. (2011) Multiple means to the same end: the genetic basis of acquired stress resistance in yeast. PLoS Genet 7: e1002353.
7. Borenstein, M., Hedges, L., Higgins, J., and Rothstein, H. (2009) Introduction to Meta-Analysis. New York, NY, USA: Wiley.
8. Borges, A.A., Jiménez-Arias, D., Expósito-Rodríguez, M., Sandalio, L.M., and Pérez, J.A. (2014) Priming crops against biotic and abiotic stresses: MSB as a tool for studying mechanisms. Front. Plant Sci 5: 1-4.
9. Brewster, J.L., de Valoir, T., Dwyer, N.D., Winter, E., and Gustin, M.C. (1993) An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763.
10. Brickner, D.G., Cajigas, I., Fondufe-Mittendorf, Y., Ahmed, S., Lee, P.C., Widom, J., etal. (2007) H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol 5: e81.
11. Brown, A.J., Budge, S., Kaloriti, D., Tillmann, A., Jacobsen, M.D., Yin, Z., etal. (2014) Stress adaptation in a pathogenic fungus. J Exp Biol 217: 144-155.
12. Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., etal. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323-337.
13. Cebrián, G., Sagarzazu, N., Pagán, R., Condón, S., and Mañas, P. (2010) Development of stress resistance in Staphylococcus aureus after exposure to sublethal environmental conditions. Int J Food Microbiol 140: 26-33.
14. Chasman, D., Ho, Y., Berry, D.B., Nemec, C.M., Macgilvray, M.E., Hose, J., etal. (2014) Pathway connectivity and signaling coordination in the yeast stress-activated signaling network. Mol Syst Biol 10: 1-24.
15. Conrath, U., Beckers, G.J.M., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., etal. (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19: 1062-1071.
16. Copas, J., and Shi, J.Q. (2000) Meta-analysis, funnel plots and sensitivity analysis. Biostatistics 1: 247-262.
17. Corrêa, A., Gurevitch, J., Martins-Loução, M.A., and Cruz, C. (2012) C allocation to the fungus is not a cost to the plant in ectomycorrhizae. Oikos 121: 449-463.
18. De Angelis, M., and Gobbetti, M. (2004) Environmental stress responses in Lactobacillus: a review. Proteomics 4: 106-122.
19. De Nadal, E., Ammerer, G., and Posas, F. (2011) Controlling gene expression in response to stress. Nat Rev Genet 12: 833-845.
20. Dhar, R., Sägesser, R., Weikert, C., and Wagner, A. (2013) Yeast adapts to a changing stressful environment by evolving cross-protection and anticipatory gene regulation. Mol Biol Evol 30: 573-588.
21. Döll, K., Chatterjee, S., Scheu, S., Karlovsky, P., and Rohlfs, M. (2013) Fungal metabolic plasticity and sexual development mediate induced resistance to arthropod fungivory. Proc R Soc B Biol Sci 280: 2013-2019.
22. Donczew, R., Zakrzewska-Zerwinska, J., and Zawilak-Pawlik, A. (2014) Beyond DnaA: The role of DNA topology and DNA methylation in bacterial replication initiation. J Mol Biol 426: 2269-2282.
23. Egger, L.A., Park, H., and Inouye, M. (1997) Signal transduction via the histidyl-aspartyl phosphorelay. Genes Cells 2: 167-184.
24. Fuchs, B.B., and Mylonakis, E. (2009) Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot Cell 8: 1616-1625.
25. Gálvez, D., and Chapuisat, M. (2014) Immune priming and pathogen resistance in ant queens. Ecol Evol 4: 1761-1767.
26. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., etal. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
27. Guan, Q., Haroon, S., Bravo, D.G., Will, J.L., and Gasch, A.P. (2012) Cellular memory of acquired stress resistance in Saccharomyces cerevisiae. Genetics 192: 495-505.
28. Guerzoni, M.E., Lanciotti, R., and Cocconcelli, P.S. (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147: 2255-2264.
29. Hastie, T., Tibshirani, R., and Friedman, J. (2011) The Elements of Statistical Learning: Data Mining, Inference, and Prediction, 2nd edn. New York, NY, USA: Springer.
30. Hayes, B.M., Anderson, M.A., Traven, A., van der Weerden, N.L., and Bleackley, M.R. (2014) Activation of stress signalling pathways enhances tolerance of fungi to chemical fungicides and antifungal proteins. Cell Mol Life Sci 71: 2651-2666.
31. Hecker, V.U. (2001) General stress response of Bacillus subtilis and other bacteria. Adv Microb Physiol 44: 35-91.
32. Hedges, L.V., Gurevitch, J., and Curtis, P.S. (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150-1156.
33. Hengge-Aronis, R. (2002) Signal transduction and regulatory mechanisms involved in control the αs (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66: 373-395.
34. Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt, S., etal. (2015) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev Camb Philos Soc. doi:10.1111/brv.12215.
35. Hohmann, S. (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
36. Jenkins, D.E., Auger, E.A., and Matin, A. (1991) Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J Bacteriol 173: 1992-1996.
37. Kundu, S., and Peterson, C.L. (2009) Role of chromatin states in transcriptional memory. Biochim Biophys Acta 1790: 445-455.
38. Lambert, G., and Kussell, E. (2014) Memory and fitness optimization of bacteria under fluctuating environments. PLoS Genet 10: e1004556.
39. Lushchak, V.I. (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol C Toxicol Pharmacol 153: 175-190.
40. McCann, M.P., Kidwell, J.P., and Matin, A. (1991) The putative 0-factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol 173: 4188-4194.
41. Martínez-Pastor, M.T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H., and Estruch, F. (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15: 2227-2235.
42. Martinez-Salazar, J.M., Sandoval-Calderón, M., Guo, X., Castillo-Ramírez, S., Reyes, A., Loza M.G., etal. (2009) The Rhizobium etli RpoH1 and RpoH2 sigma factors are involved in different stress responses. Microbiology-Sgm 155: 386-397.
43. Mitchell, A., and Pilpel, Y. (2011) A mathematical model for adaptive prediction of environmental changes by microorganisms. PNAS 108: 7271-7276.
44. Mitchell, A., Romano, G.H., Groisman, B., Yona, A., Dekel, E., Kupiec, M., etal. (2009) Adaptive prediction of environmental changes by microorganisms. Nature 460: 220-224.
45. Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I., and Brown, A.J.P. (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9: 44.
46. Noventa-Jordão, M.A., Couto, R.M., Goldman, M.H.S., Aguirre, J., Iyer, S., Caplan, A., etal. (1999) Catalase activity is necessary for heat-shock recovery in Aspergillus nidulans germlings. Microbiology 145: 3229-3234.
47. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
48. Rillig, M.C., Rolff, J., Tietjen, B., Wehner, J., and Andrade-Linares, D.R. (2015) Community priming-effects of sequential stressors on microbial assemblages. FEMS Microbiol Ecol 91: fiv040.
49. Rosenberg, M.S., Adams, D.C., and Gurevitch, J. (2000) MetaWin: Statistical Software for Meta-Analysis, Version 2.0. Sunderland, MA, USA: Sinauer Associates.
50. Ruijter, G.J.G., Bax, M., Patel, H., Flitter, S.J., van de Vondervoort, P.J.I., de Vries, R.P., etal. (2003) Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryot Cell 2: 690-698.
51. Schimel, J., Balser, T.C., and Wallenstein, M. (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88: 1386-1394.
52. Singer, M.A., and Lindquist, S. (1998) Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1: 639-648.
53. Smith, D.A., Morgan, B.A., and Quinn, J. (2010) Stress signalling to fungal stress-activated protein kinase pathways. FEMS Microbiol Lett 306: 1-8.
54. Stanley, D., Bandara, A., Fraser, S., Chambers, P.J., and Stanley, G.A. (2010) The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. J Appl Microbiol 109: 13-24.
55. Tamai, K.T., Liu, X., Silar, P., Sosinowski, T., and Thiele, D.J. (1994) Heat shock transcription factor activates yeast metallothionein gene expression in response to heat and glucose starvation via distinct signalling pathways. Mol Cell Biol 14: 8155-8165.
56. Tidbury, H.J., Best, A., and Boots, M. (2012) The epidemiological consequences of immune priming. Proc R Soc B Biol Sci 279: 4505-4512.
57. Treseder, K.K., and Lennon, J.T. (2015) Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev 79: 243-262.
58. Trollmo, C., André, L., Blomberg, A., and Adler, L. (1988) Physiological overlap between osmotolerance and thermotolerance in Saccharomyces cerevisiae. FEMS Microbiol Lett 56: 321-326.
59. Verghese, J., Abrams, J., Wang, Y., and Morano, K.A. (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76: 115-158.
60. Weber, H., Polen, T., Heuveling, J., Wendisch, V.F., and Hengge, R. (2005) Genome-wide analysis of the general stress response network in Escherichia coli: σS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187: 1591-1603.
61. Wolf, D.M., Fontaine-Bodin, L., Bischofs, I., Price, G., Keasling, J., and Arkin, A.P. (2008) Memory in microbes: quantifying history-dependent behavior in a bacterium. PLoS ONE 3: e1700.
62. Zacharioudakis, L., Gligorls, T., and Tzamarias, D. (2007) A yeast catabolic enzyme controls transcriptional memory. Curr Biol 17: 2041-2046.
63. Zakrzewska, A., van Eikenhorst, G., Burggraaff, J.E.C., Vis, D.J., Hoefsloot, H., Delneri, D., etal. (2011) Genome-wide analysis of yeast stress survival and tolerance acquisition to analyze the central trade-off between growth rate and cellular robustness. Mol Biol Cell 22: 4435-4446.
64. Zaman, S., Lippman, S.I., Zhao, X., and Broach, J.R. (2008) How Saccharomyces responds to nutrients. Annu Rev Genet 42: 27-81.
65. Zuur, A., Ieno, E.N., Walker, N., Saveliev, A.A., and Smith, G.M. (2009) Mixed Effects Models and Extensions in Ecology with R. New York, NY, USA: Springer.