Abstract
Bacterial metabolites with communicative functions could provide protection against stress conditions to members of the same species. Yet, information remains limited about protection provided by metabolites in Bacillus cereus and inter-species. This study investigated the effect of extracellular compounds derived from heat shocked (HS) and non-HS cultures of B. cereus and Geobacillus stearothermophilus on the thermotolerance of non-HS vegetative and sporulating B. cereus. Cultures of B. cereus and G. stearothermophilus were subjected to HS (42 or 65 °C respectively for 30 min) or non-HS treatments. Cells and supernatants were separated, mixed in a combined array, and then exposed to 50 °C for 60 min and viable cells determined. For spores, D values (85 and 95 °C) were evaluated after 120 h. In most cases, supernatants from HS B. cereus cultures added to non-HS B. cereus cells caused their thermotolerance to increase (D 50 12.2–51.9) when compared to supernatants from non-HS cultures (D 50 7.4–21.7). While the addition of supernatants from HS and non-HS G. stearothermophilus cultures caused the thermotolerance of non-HS cells from B. cereus to decrease initially (D 50 3.7–7.1), a subsequent increase was detected in most cases (D 50 18–97.7). In most cases, supernatants from sporulating G. stearothermophilus added to sporulating cells of B. cereus caused the thermotolerance of B. cereus 4810 spores to decline, whereas that of B. cereus 14579 increased. This study clearly shows that metabolites in supernatants from either the same or different species (such as G. stearothermophilus) influence the thermotolerance of B. cereus.
Similar content being viewed by others
References
Bunning VK, Crawford RG, Tierney JT, Peeler JT (1990) Thermotolerance of Listeria monocytogenes and Salmonella typhimurium after sublethal heat shock. Appl Environ Microbiol 56:3216–3219
Ceuppens S, Uyttendaele M, Drieskens K, Rajkovic A, Boon N, Wiele TV (2012) Survival of Bacillus cereus vegetative cells and spores during in vitro simulation of gastric passage. J Food Protect 75:690–694
Chen ST (2002) Proteomic study of cold shock protein in Bacillus stearothermophilus P1: comparison of temperature downshifts. Proteomics 2:1316–1324
Clavel T, Carlin F, Lairon D, Nguyen-The C, Schmitt P (2004) Survival of Bacillus cereus spores and vegetative cells in acid media simulating human stomach. J Appl Microbiol 97:214–219
Comella N, Grossman AD (2005) Conservation of genes and processes controlled by the quorum response in bacteria: characterization of genes controlled by the quorum-sensing transcription factor ComA in Bacillus subtilis. Mol Microbiol 57:1159–1174
Derekova A, Sjøholm C, Mandeva R, Michailova L, Kambourova M (2006) Biosynthesis of a thermostable gellan lyase by newly isolated and characterized strain of Geobacillus stearothermophilus 98. Extremophiles 10:321–326
Frenzel E, Doll V, Pauthner M, Lücking G, Scherer S, Ehling-Schulz M (2012) CodY orchestrates the expression of virulence determinants in emetic Bacillus cereus by impacting key regulatory circuits. Mol Microbiol 85:67–88
Garcia-Alvarado JS, Labbe RG, Rodriguez MA (1992) Sporulation and enterotoxin production of Clostridium perfringens type A at 37 and 43C. Appl Environ Microbiol 58:1411–1414
Georget E, Kapoor S, Winter R, Reineke K, Song Y, Callanan M, Ananta E, Heinz V, Mathys A (2014) In situ investigation of Geobacillus stearothermophilus spore germination and inactivation mechanisms under moderate high pressure. Food Microbiol 41:8–18
Hawumba JF, Theron J, Brözel VS (2002) Thermophilic protease-producing Geobacillus from Buranga hot springs in Western Uganda. Curr Microbiol 45:144–150
Heredia NL, García GA, Luévanos R, Labbé RG, García-Alvarado JS (1997) Elevation of the heat resistance of vegetative cells and spores of Clostridium perfringens type A by sublethal heat shock. J Food Protect 60:998–1000
Heredia N, Ybarra P, Hernández C, García S (2009) Extracellular protectants produced by Clostridium perfringens cells at elevated temperatures. Lett Appl Microbiol 48:133–139
Huillet E, Tempelaars MH, André-Leroux G, Wanapaisan P, Bridoux L, Makhzami S, Panbangred W, Martin-Verstraete I, Abee T, Lereclus D (2012) PlcRa, a new quorum-sensing regulator from Bacillus cereus plays a role in oxidative stress responses and cysteine metabolism in stationary phase. PLoS One 7:e51047
Kanjee U, Ogata K, Houry WA (2012) Direct binding targets of the stringent response alarmone (p) ppGpp. Mol Microbiol 85:1029–1043
Koch B, Kilstrup M, Vogensen FK, Hammer K (1998) Induced levels of heat shock proteins in dnaK mutant of Lactococcus lactis. J Bacteriol 180:3873–3881
Krüger E, Hecker M (1988) The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J Bacteriol 180: 6681–6688
Lee NK, Yeo IC, Park JW, Hahm YT (2011) Growth inhibition and induction of stress protein, GroEL, of Bacillus cereus exposed to antibacterial peptide isolated from Bacillus subtilis SC-8. Appl Biochem Biotechnol 165:235–242
Liu P, Ewis HE, Tai PC, Lu CD, Weber IT (2007) Crystal structure of the Geobacillus stearothermophilus carboxylesterase Est55 and its activation of prodrug CPT-11. J Mol Biol 367:212–223
Mamo G, Gashe BA, Gessesse A (1999) A highly thermostable amylase from a newly isolated thermophilic Bacillus sp. WN11. J Appl Environ Microbiol 86:557–560
Messaoud EB, Ammar YB, Mellouli L, Bejar S (2002) Thermostable pullulanase type I from new isolated Bacillus thermoleovorans US105: cloning, sequencing and expression of the gene in E. coli. Enzyme Microb Tech 31(6):827–832
Movahedi S, Waites W (2002) Cold shock response in sporulating Bacillus subtilis and its effect on spore heat resistance. J Bacteriol 184:5275–5281
Nikolaev YA, Borzenkov IA, Tarasov AL, Loiko NG, Kozlova AN, Gal’chenko VF, El’-Registan GI (2010) Role of alkylhydroxybenzenes in bacterial adaptation to unfavorable growth conditions. Microbiology 79:747–752
Periago PM, Fernández PS, Ocio MJ, Martínez A (1998) Apparent thermal resistance of Bacillus stearothermophilus spores recovered under anaerobic conditions. Z Lebensm Unters For 206:63–67
Periago PM, van Schaik W, Abee T, Wouters JA (2002) Identification of proteins involved in the heat stress response of Bacillus cereus ATCC 14579. Appl Environ Microbiol 68:3486–3495
Pokusaeva K, Kuisiene N, Jasinskyte D, Rutiene K, Saleikiene J, Chitavichius D (2009) Novel bacteriocins produced by Geobacillus stearothermophilus. Cent Eur J Biol 4:196–203
Rhimi M, Juy M, Aghajari N, Haser R, Bejar S (2007) Probing the essential catalytic residues and substrate affinity in the thermoactive Bacillus stearothermophilus US100 L-arabinose isomerase by site-directed mutagenesis. J Bacteriol 189:3556–3563
Rowbury RJ (2005) Intracellular and extracellular components as bacterial thermometers, and early warning against thermal stress. Sci Prog 88:71–99
Ryan RP, Dow JM (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154:1845–1858
Samapundo S, Heyndrickx M, Xhaferi R, Devlieghere F (2011) Validated empirical models describing the combined effect of water activity and pH on the heat resistance of spores of a psychrotolerant Bacillus cereus strain in broth and Béchamel sauce. J Food Protect 74:1662–1669
Schaeffer P (1969) Sporulation and the production of antibiotics, exoenzymes, and exotoxins. Bacteriol Rev 33:48–71
Schumann W (2003) The Bacillus subtilis heat shock stimulon. Cell Stress Chaperon 8:207–217
Setlow P (2011) Resistances of bacterial spores. In: Storz G, Hengge R (eds) Bacterial stress responses, 2nd edn. American Society for Microbiology Press, Washington, DC
Soliman NA, Knoll M, Abdel-Fattah YR, Schmid RD, Lange S (2007) Molecular cloning and characterization of thermostable esterase and lipase from Geobacillus thermoleovorans YN isolated from desert soil in Egypt. Process Biochemist 42:1090–1100
Stepanenko IY, Mulyukin A, Kozlova A, Nikolaev YA (2005) The role of alkylhydroxybenzenes in the adaptation of Micrococcus luteus to heat shock. Microbiology 74:20–26
Straight PD, Kolter R (2009) Interspecies chemical communication in bacterial development. Annu Rev Microbiol 63:99–118
Sturme MH, Kleerebezem M, Nakayama J, Akkermans AD, Vaughan EE, de Vos WM (2002) Cell to cell communication by autoinducing peptides in gram-positive bacteria. Anton Leeuwenhoek 81:233–243
Umezawa H (1982) Low molecular weight enzyme inhibitors of microbial origin. Annu Rev Microbiol 36:75–99
Usaga J, Worobo RW, Padilla-Zakour OI (2014) Effect of acid adaptation and acid shock on thermal tolerance and survival of Escherichia coli O157: H7 and O111 in apple juice. J Food Protect 77:1656–1663
van der Veen S, Abee T (2010) HrcA and DnaK are important for static and continuous-flow biofilm formation and disinfectant resistance in Listeria monocytogenes. Microbiology 156:3782–3790
Weichart DH, Kell DB (2001) Characterization of an autostimulatory substance produced by Escherichia coli. Microbiology 147:1875–1885
Xu D, Côte JC (2003) Phylogenetic relationships between Bacillus species and related genera inferred from comparison of 3′ end 16S rDNA and 5′ end 16S–23S ITS nucleotide sequences. Int J Syst Evol Micr 53:695–704
Acknowledgements
This work was supported by a grant from the Consejo Nacional de Ciencia y Tecnología de México (CONACYT) grant no. 156073 and the Universidad Autónoma de Nuevo León. M.G. acknowledges a postgraduate fellowship from CONACYT.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gómez-Govea, M.A., García, S. & Heredia, N. Bacterial metabolites from intra- and inter-species influencing thermotolerance: the case of Bacillus cereus and Geobacillus stearothermophilus . Folia Microbiol 62, 183–189 (2017). https://doi.org/10.1007/s12223-016-0487-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-016-0487-2