Abstract
Bacillus cereus 905, originally isolated from wheat rhizosphere, exhibits strong colonization ability on wheat roots. Our previous studies showed that root colonization is contributed by the ability of the bacterium to efficiently utilize carbon sources and form biofilms and that the sodA2 gene-encoded manganese-containing superoxide dismutase (MnSOD2) plays an indispensable role in the survival of B. cereus 905 in the wheat rhizosphere. In this investigation, we further demonstrated that the ability of B. cereus 905 to resist adverse environmental conditions is partially attributed to activation of the alternative sigma factor σB, encoded by the sigB gene. The sigB mutant experienced a dramatic reduction in survival when cells were exposed to ethanol, acid, heat, and oxidative stress or under glucose starvation. Analysis of the sodA2 gene transcription revealed a partial, σB-dependent induction of the gene during glucose starvation or when treated with paraquat. In addition, the sigB mutant displayed a defect in biofilm formation under stress conditions. Finally, results from the root colonization assay indicated that sigB and sodA2 collectively contribute to B. cereus 905 colonization on wheat roots. Our study suggests a diverse role of SigB in rhizosphere survival and root colonization of B. cereus 905 under stress conditions.
Key points
• SigB confers resistance to environmental stresses in B. cereus 905.
• SigB plays a positive role in glucose utilization and biofilm formation in B. cereus.
• SigB and SodA2 collectively contribute to colonization on wheat roots by B. cereus.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. Eur J Plant Pathol 114:329–341. https://doi.org/10.1007/s10658-005-0233-0
Ali S, Hameed S, Imran A, Iqbal M (2014) Genetic, physiological and biochemical characterization of Bacillus sp. strain RMB7 exhibiting plant growth promoting and broad spectrum antifungal activities. Microb Cell Fact 14:144. https://doi.org/10.1186/PREACCEPT-6657919731258908
Antelmann H, Engelmann S, Schmid R, Hecker M (1996) General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon. J Bacteriol 178:6571–6578. https://doi.org/10.1128/jb.178.22.6571-6578.1996
Azizoglu RO, Kathariou S (2010) Temperature-dependent requirement for catalase in aerobic growth of Listeria monocytogenes F2365. Appl Environ Microbiol 76:6998–7003. https://doi.org/10.1128/AEM.01223-10
Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiology 134:307–319. https://doi.org/10.1104/pp.103.028712
Barabote RD, Saier MH (2005) Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69:608–634. https://doi.org/10.1128/MMBR.69.4.608-634.2005
Benson AK, Haldenwang WG (1993) Regulation of σB levels and activity in Bacillus subtilis. J Bacteriol 175:2347–2356. https://doi.org/10.1007/BF00004028
Bernhardt J, Völker U, Völker A, Antelmann H, Schmid R, Mach H, Hecker M (1997) Specific and general stress proteins in Bacillus subtilis-a two-dimensional protein electrophoresis study. Microbiology 143:999–1017. https://doi.org/10.1099/00221287-143-3-999
Bonilla CY (2020) Generally stressed out bacteria: environmental stress response mechanisms in Gram-positive bacteria. Inteqr Comp Biol 60:126–133. https://doi.org/10.1093/icb/icaa002
Brody MS, Price CW (1998) Bacillus licheniformis sigB operon encoding the general stress transcription factor σB. Gene 212:111–118. https://doi.org/10.1016/S0378-1119(98)00140-1
Cebrián G, Arroyo C, Condón S, Mañas P (2015) Osmotolerance provided by the alternative sigma factors σB and rpoS to Staphylococcus aureus and Escherichia coli is solute dependent and does not result in an increased growth fitness in NaCl containing media. Int J Food Microbiol 214:83–90. https://doi.org/10.1016/j.ijfoodmicro.2015.07.011
Chan PF, Foster SJ, Ingham E, Clements MO (1998) The Staphylococcus aureus alternative sigma factor sigmaB controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model. J Bacteriol 180:6082–6089. https://doi.org/10.1590/S0103-90161994000100011
Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo J-H (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15:848–864. https://doi.org/10.1111/j.1462-2920.2012.02860.x
Chowdhury SP, Uhl J, Grosch R, Alqueres S, Pittroff S, Dietel K, Schmitt-Kopplin P, Borriss R, Hartmann A (2015) Cyclic lipopeptides of Bacillus amyloliquefaciens subsp. plantarum colonizing the lettuce rhizosphere enhance plant defense responses toward the bottom rot pathogen Rhizoctonia solani. Mol Plant Microbe In 28:984–995. https://doi.org/10.1094/mpmi-03-15-0066-r
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. https://doi.org/10.1016/j.soilbio.2009.11.024
Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant disease: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. https://doi.org/10.1128/AEM.71.9.4951-4959.2005
Ding H, Niu B, Fan H, Li Y, Wang Q (2016) Draft genome sequence of Bacillus cereus 905, a plant growth-promoting rhizobacterium of wheat. Genome Announc 4:e00489–e00416. https://doi.org/10.1128/genomeA.00489-16
Fan H, Zhang Z, Li Y, Zhang X, Duan Y, Wang Q (2017) Biocontrol of bacterial fruit blotch by Bacillus subtilis 9407 via surfactin-mediated antibacterial activity and colonization. Front Microbiol 8:1973. https://doi.org/10.3389/fmicb.2017.01973
Ferreira A, O'Byrne CP, Boor KJ (2001) Role of σB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Appl Environ Microbiol 67:4454–4457. https://doi.org/10.1128/aem.67.10.4454-4457.2001
Gao T, Ding M, Yang C-H, Fan H, Chai Y, Li Y (2019) The phosphotransferase system gene ptsH plays an important role in MnSOD production, biofilm formation, swarming motility, and root colonization in Bacillus cereus 905. Res Microbiol 170:86–96. https://doi.org/10.1016/j.resmic.2018.10.002
Gao T, Foulston L, Chai Y, Wang Q, Losick R (2015) Alternative modes of biofilm formation by plant-associated Bacillus cereus. MicrobiologyOpen 4:452–464. https://doi.org/10.1002/mbo3.251
Gao T, Li Y, Ding M, Chai Y, Wang Q (2017) The phosphotransferase system gene ptsI in Bacillus cereus regulates expression of sodA2 and contributes to colonization of wheat roots. Res Microbiol 168:524–535. https://doi.org/10.1016/j.resmic.2017.04.003
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117. https://doi.org/10.1139/m95-015
Guldimann C, Boor KJ, Wiedmann M, Guariglia-Oropeza V (2016) Resilience in the face of uncertainty: Sigma factor B fine-tunes gene expression to support homeostasis in Gram-positive bacteria. Appl Environ Microbiol 82:4456–4469. https://doi.org/10.1128/aem.00714-16
Hecker M, Pané-Farré J, Völker U (2007) SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Ann Rev Microbiol 61:215–236. https://doi.org/10.1146/annurev.micro.61.080706.093445
Horsburgh M, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ (2002) σB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184:5457–5467. https://doi.org/10.1128/jb.184.19.5457-5467.2002
Huang Y, Morvay AA, Shi X, Suo Y, Shi C, Knøchel S (2018) Comparison of oxidative stress response and biofilm formation of Listeria monocytogenes serotypes 4b and 1/2a. Food Control 85:416–422. https://doi.org/10.1016/j.foodcont.2017.10.007
Kalma SM, Duncan ML, Thomas SM, Price CW (1990) Similar organization of the sigB and spoIIA operons encoding alternate sigma factors of Bacillus subtilis RNA polymerase. J Bacteriol 172:5575–5585. https://doi.org/10.1128/jb.172.10.5575-5585.1990
Kim YC, Miller CD, Anderson AJ (2000) Superoxide dismutase activity in Pseudomonas putida affects utilization of sugars and growth on root surfaces. Appl Environ Microbiol 66:1460–1467. https://doi.org/10.1128/aem.66.4.1460-1467.2000
Mitchell G, Brouillette E, Séguin DL, Asselin A-E, Jacob CL, Malouin F (2010) A role for sigma factor B in the emergence of Staphylococcus aureus small-colony variants and elevated biofilm production resulting from an exposure to aminoglycosides. Microb Pathogenesis 48:18–27. https://doi.org/10.1016/j.micpath.2009.10.003
Niu B, Vater J, Rueckert C, Blom J, Lehmann M, Ru J-J, Chen X-H, Wang Q, Borriss R (2013) Polymyxin P is the active principle in suppressing phytopathogenic Erwinia spp. by the biocontrol rhizobacterium Paenibacillus polymyxa M-1. BMC Microbiol 13:137. https://doi.org/10.1186/1471-2180-13-137
Petersohn A, Brigulla M, Haas S, Hoheisel JD, Volker U, Hecker M (2001) Global analysis of the general stress response of Bacillus subtilis. J Bacteriol 183:5617–5631. https://doi.org/10.1128/jb.183.19.5617-5631.2001
Ramírez-Guadiana FH, Barajas-Ornelas RC, Corona-Bautista SU, Setlow P, Pedraza-Reyes M (2016) The RecA-dependent SOS response is active and required for processing of DNA damage during Bacillus subtilis sporulation. PLoS One 11:e0150348. https://doi.org/10.1371/journal.pone.0150348
Qin Y, Shang Q, Zhang Y, Li P, Chai Y (2017) Bacillus amyloliquefaciens L-S60 reforms the rhizosphere bacterial community and improves growth conditions in cucumber plug seedling. Front Microbiol 8:2620. https://doi.org/10.3389/fmicb.2017.02620
Saier MH, Reizer J (1994) The bacterial phosphotransferase system: new frontiers 30 years later. Mol Microbiol 13:755–764. https://doi.org/10.1111/j.1365-2958.1994.tb00468.x
Salvetti S, Faegri K, Ghelardi E, Klost A-B, Senesi S (2011) Global gene expression profile for swarming Bacillus cereus bacteria. Appl Environ Microbiol 77:5149–5156. https://doi.org/10.1128/AEM.00245-11
Schulte C, Arenskötter M, Berekaa MM, Arenskötter Q, Priefert H, Steinbüchel A (2008) Possible involvement of an extracellular superoxide dismutase (SodA) as a radical scavenger in poly(cis-1,4-isoprene) degradation. Appl Environ Microbiol 74:7643–7653. https://doi.org/10.1128/AEM.01490-08
Sue D, Fink D, Wiedmann M, Boor KJ (2004) σB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150:3843–3855. https://doi.org/10.1099/mic.0.27257-0
Suo Y, Liu Y, Zhou X, Huang Y, Shi C, Matthews K, Shi X (2014) Impact of sod on the expression of stress-related genes in Listeria monocytogenes 4b G with/without paraquat treatment. J Food Sci 79:M1745–M1749. https://doi.org/10.1111/1750-3841.12545
Supa-amornkul S, Mongkolsuk P, Summpunn P, Chaiyakunvat P, Navaratdusit W, Jiarpinitnun C, Chaturongakul S (2019) Alternative sigma factor B in bovine mastitis-causing Staphylococcus aureus: characterization of its role in biofilm formation, resistance to hydrogen peroxide stress, regulon members. Front Microbiol. 10. https://doi.org/10.3389/fmicb.2019.02493
Sutrina SL, McGeary T, Bourne C-A (2007) The phosphoenolpyruvate: sugar phosphotransferase system and biofilms in Gram-positive bacteria. J Mol Microbiol Biotechnol 12:269–272. https://doi.org/10.1159/000099648
Thakur A, Kumar P, Lata J, Devi N, Chand D (2018) Thermostable Fe/Mn superoxide dismutase from Bacillus licheniformis SPB-13 from thermal springs of Himalayan region: purification, characterization and antioxidative potential. Int J Biol Macromol 115:1026–1032. https://doi.org/10.1016/j.ijbiomac.2018.04.155
Tuchscherr L, Bischoff M, Lattar SM, Noto Llana M, Pförtner H, Niemann S, Geraci J, Van de Vyver H, Fraunholz MJ, Cheung AL, Herrmann M, Völker U, Sordelli DO, Peters G, Löffler B (2015) Sigma factor SigB is crucial to mediate Staphylococcus aureus adaptation during chronic infections. PLoS Pathog 11:e1004870. https://doi.org/10.1371/journal.ppat.1004870
Völker U, Maul B, Hecker M (1999) Expression of the σB-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. J Bacteriol 181:3942–3948. https://doi.org/10.1007/s13353-014-0252-7
van Schaik W, Abee T (2005) The role of σB in the stress response of Gram-positive bacteria-targets for food preservation and safety. Curr Opin Biotech 16:218–224. https://doi.org/10.1016/j.copbio.2005.01.008
van Schaik W, Tempelaars MH, Wouters JA, de Vos WM, Abee T (2004) The alternative sigma factor sigma σB of Bacillus cereus: response to stress and role in heat adaptation. J Bacteriol 186:316–325. https://doi.org/10.1128/jb.186.2.316-325.2004
Wang S, Chang L-Y, Wang Y-J, Wang Q, Yang C-H, Mei R-H (2009a) Nanoparticles affect the survival of bacteria on leaf surfaces. FEMS Microbiol Ecol 68:182–191. https://doi.org/10.1111/j.1574-6941.2009.00664.x
Wang SW, Chen CY, Tseng JT, Liang SH, Chen SC, Hsieh C, Chen YH, Chen CC (2009b) orf4 of the Bacillus cereus sigB gene cluster encodes a general stress-inducible Dps-like bacterioferritin. J Bacteriol 191:4522–4533. https://doi.org/10.1128/JB.00272-09
Wang Y, Wang H, Yang CH, Wang Q, Mei R (2007) Two distinct manganese-containing superoxide dismutase genes in Bacillus cereus: their physiological characterizations and roles in surviving in wheat rhizosphere. FEMS Microbiol Lett 272:206–213. https://doi.org/10.1111/j.1574-6968.2007.00759.x
Weng J, Wang Y, Li J, Shen Q, Zhang R (2013) Enhanced root colonization and biocontrol activity of Bacillus amyloliquefaciens SQR9 by arbB gene disruption. Appl Microbiol Biotechnol 97:8823–8830. https://doi.org/10.1007/s00253-012-4572-4
Xu S, Yang N, Zheng S, Yan F, Jiang C-H, Yu Y, Guo J-H, Chai Y, Chen Y (2018) The spo0A-sinI-sinR regulatory circuit plays an essential role in biofilm formation, nematicidal activities, and plant protection in Bacillus cereus AR156. Mol Plant Microb In 30:603–619. https://doi.org/10.1094/mpmi-02-17-0042-r
Xu YB, Chen M, Zhang Y, Wang M, Wang Y, Huang QB, Wang X, Wang G (2014) The phosphotransferase system gene ptsI in the endophytic bacterium Bacillus cereus is required for biofilm formation, colonization, and biocontrol against wheat sharp eyespot. FEMS Microbiol Lett 354:142–152. https://doi.org/10.1111/1574-6968.12438
Zeng Q, Xie J, Li Y, Gao T, Xu C, Wang Q (2018) Comparative genomic and functional analyses of four sequenced Bacillus cereus genomes reveal conservation of genes relevant to plant-growth-promoting traits. Sci Rep 8:17009. https://doi.org/10.1038/s41598-018-35300-y
Zeriouh H, de Vicente A, Perez-Garcia A, Romero D (2014) Surfactin triggers biofilm formation of Bacillus subtilis in melon phylloplane and contributes to the biocontrol activity. Environ Microbiol 16:2196–2211. https://doi.org/10.1111/1462-2920.12271
Funding
This research was financially supported by grants from the Program of Science and Technology of Beijing Municipal Education Commission, China (KM202010020014) and a Science Fund for Young Scholars from the Beijing University of Agriculture to T. Gao (No. SXQN201902).
Author information
Authors and Affiliations
Contributions
TG, YL, and QW conceived and designed the research. TG conducted the main experiments and data analysis and wrote a manuscript draft. MD did some data analysis. YL and QW guided the experimental design and performed the data analysis. YC analyzed the experimental data. TG, YC, and QW wrote the final version of the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gao, T., Li, Y., Chai, Y. et al. SigB regulates stress resistance, glucose starvation, MnSOD production, biofilm formation, and root colonization in Bacillus cereus 905. Appl Microbiol Biotechnol 105, 5943–5957 (2021). https://doi.org/10.1007/s00253-021-11402-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-021-11402-y