Effect of pH and temperature on the growth and antagonistic activity of Bacillus subtilis on Rhizoctonia solani

Rocío Jiménez-Delgadillo, Silvia Edith Valdés-Rodríguez, Víctor Olalde-Portugal, Rosario Abraham-Juárez, José Luis García-Hernández

Abstract


In this study, the effects of environmental conditions (pH and temperature) on the growth rate and the inhibitory effect of different strains of Bacillus subtilis on Rhizoctonia solani were evaluated. Strains of B. subtilis were grown in potato infusion broth. The physiological behavior and the growth rate (dN / dt) of the strains were analyzed under different pH and temperature conditions. The strains behaved differently, which allowed establishing optimum and suboptimal growth conditions for each strain. Cell-free supernatants obtained under different growth conditions were used in a quantitative test of in vitro antagonist activity against R. solani. This study showed that the inhibitory effect of the strains occurs mainly in the stationary phase.


Keywords


biocontrol; growth rate; antagonism; physiological state

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References


Ahlem H, Mohammed E, Badoc A and Ahmed L. 2012. Effect of pH, temperature and water activity on the inhibition of Botrytis cinerea by Bacillus amyloliquefaciens isolates. African Journal of Biotechnology 11:2210-2217. Disponible en línea: http://www.academicjournals.org/AJB DOI: 10.5897/AJB11.645

Ashlee M, Losick ER and Kolter R. 2008. Ecology and genomics of Bacillus subtilis. Trends in Microbiology 16:269-275. https://doi.org/10.1016/j.tim.2008.03.004

Ashlee M, Losick ER and Kolter R. 2007. Bacillus subtilis Genome Diversity. Journal. Bacteriology 189:1163-1170. Disponible en línea: http://jb.asm.org/content/189/3/1163.short

Bais HP, Fall R and 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

Bais HP, Weir TF, Perry LG, Gilroy S and Vivanco JM. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57:233-266. https://doi.org/10.1146/annurev.arplant.57.032905.105159

Bapat S and Shah AK. 2000. Biological control of fusarial wilt of pigeon pea by Bacillus brevis. Canadian Journal of Microbiology 46:25-132. https://doi.org/10.1139/w99-109

Bernal G, Illanes A and Ciampi L. 2002. Isolation and partial purification of a metabolite from a mutant strain of Bacillus sp. with antibiotic activity against plant pathogenic agents. Electronic Journal of Biotechnology 5:12-20. Disponible en línea: http://www.scielo.cl/pdf/ejb/v5n1/04.pdf

Bloemberg G and Lugtenberg B. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Current Opinion Plant Biology 4:343-350. https://doi.org/10.1016/S1369-5266(00)00183-7

Castro SS, Herschkovitz Y, Okon Y and Jurkevitch E. 2007. Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms. Microbiology Letters 276:1-11. https://doi.org/10.1111/j.1574-6968.2007.00878.x

Compant S, Duffy B, Nowak J, Clement C and Ait Barka E. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: Principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology 71:4951-4959. https//doi.org/10.1128/AEM.71.9.4951-4959.2005

Conn VM and Franco CMM. 2004. Effect of microbial inoculants on the indigenous actinobacterial endophyte population in the roots of wheat as determined by terminal restriction fragment length polymorphism. Applied and Environmental Microbiology 70:6407-6413. https://doi.org/10.1128/AEM.70.11.6407-6413.2004

Cosby WM, Vollenbroich D, Lee OH and Zuber P. 1998. Altered srf expression in Bacillus subtilis resulting from changes in culture pH is dependent on the Spo0k oligopeptide permease and the ComQX system of extracellular compounds. Journal of Bacteriology 180:1438-1445. Disponible en línea: http://jb.asm.org/content/180/6/1438.short

Costa E, Usall J, Teixido N, Delgado J and Viñas I. 2002. Water activity, temperature and pH effects on growth of the biocontrol agent Pantoea agglomerans CPA-2. Canadian Journal of Microbiology 48:1082-1088. https://doi.org/10.1139/w03-001

Fujinami S and Fujisawa M. 2010. Industrial applications of alkaliphiles and their enzymes-past, present and future. Environmental Technology 31:845-856. http://dx.doi.org/10.1080/09593331003762807

Goddard VJ, Bailey MJ, Darrah P, Lilley AK and Thompson IP. 2001. Monitoring temporal and spatial variation in rhizosphere bacterial population diversity: a community approach for the improved selection of rhizosphere competent bacteria. Plant and Soil 232:181-193. https://doi.org/10.1023/A:1010302607616

Gong M, Wang JD, Zhang J, Yang H, Lu XF, Pei Y and Cheng JQ. 2006. Study of the antifungal ability of Bacillus subtilis strain PY-1 in vitro and identification of its antifungal substance (Iturin A). Acta Biochimica et Biophysica Sinica 38:233-240. https://doi.org/10.1111/j.1745-7270.2006.00157.x

Grahovac JA, Ron?evi? ZZ, Tadijan IŽ, Joki? AI and Dodi? JM. 2015. Optimization of media for antimicrobial compounds production by Bacillus subtilis. Acta Alimentaria 44:427-435. DOI: 10.1556/066.2015.44.0014

Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T and Achouak W. 2008. Plant host habitat and root exudates shape soil bacterial community structure. The ISME Journal 2:1221-1230. https//doi.org/10.1038/ismej.2008.80

Horswill AR, Stoodley P, Stewart PS and Parsek MR. 2007. The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Analytical and Bioanalytical Chemistry 387:371-380. https://doi.org/10.1007/s00216-006-0720-y

Johnson LF and Curl EA. 1972. Culture media. In Methods for research on the ecology of soil borne plant pathogens. Burgges Publishing Company Auburn, Alabama 16:187-208. Disponible en línea: https://www.cabdirect.org/cabdirect/abstract/19731903549

Jones SW, Dobson ME, Francesconi SC, Schoske R and Crawford R. 2005. DNA assays for detection, identification, and Individualization of select agent microorganisms. Croatian Medical Journal 46:522-529. Disponible en línea: http://neuron.mefst.hr/docs/CMJ/issues/2005/46/4/16100754.pdf

Kamnev AA. 2008. FTIR spectroscopic studies of bacterial cellular responses to environmental factors, plant-bacterial interactions and signalling. Journal of Spectroscopy 22:83-95. http://dx.doi.org/10.3233/SPE-2008-0329

Kim PLL, Ryu J, Kim YH and ChI YT. 2010. Production of biosurfactant lipopeptides Iturin A, fengycin, and surfactin a from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. Journal Microbiology and Biotechnology 20:138-145. http//doi.org/10.4014/jmb.0905.05007

Kozdrój J and Van Elsas JD. 2000. Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biology and Biochemistry 32:1405-1417. https://doi.org/10.1016/S0038-0717(00)00058-4

Kröber M, Verwaaijen B, Wibberg D, Winkler A, Pühler A and Schlüter A. 2016. Comparative transcriptome analysis of the biocontrol strain Bacillus amyloliquefaciens FZB42 as response to biofilm formation analyzed by RNA sequencing. Journal Biotechnology 231:212-223. DOI: 10.1016/j.jbiotec.2016.06.013

Leclére V, Béchet M, Adam A, Guez JS, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M and Jacques P. 2005. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Applied and Environmental Microbiology 71:4577-4584. https://doi.org/10.1128/AEM.71.8.4577-4584.2005

Matarante A, Baruzzi F, Cocconcelli PS and Morea M. 2004. Genotyping and toxigenic potential of Bacillus subtilis and Bacillus pumilus strains occurring in industrial and artisanal cured sausages. Applied and Environmental Microbiology 70:5168-5176. https://doi.org/10.1128/AEM.70.9.5168-5176.2004

Nagórska K, Bikowski M and Obuchowski M. 2007. Multicellular behaviour and production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent. Acta Biochimica Polonica 54:495-508. Disponible en línea: https://www.ncbi.nlm.nih.gov/pubmed/17882321

O´Callagman M, Gerrard EM and Johnson VW. 2001. New Zeland Plant Protection 54:128-135. Disponible en línea: https://nzpps.org/journal/54/nzpp_541280.pdf

Ongena M and Jacques P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiology 16:116-125. DOI: 10.1016/j.tim.2007.12.009

Pal KK and B. Mc Spadden Gardener. 2006. Biological Control of Plant Pathogens. The Plant Health Instructor. DOI: 10.1094/PHI-A-2006-1117-02

Rey MW, Ramaiya P, Nelson BA, Brody-Karpin SD, Zaretsky EJ, Tang M, López de León A, Xiang H, Gusti V, Clausen IG, Olsen PB, Rasmussen MD, Andersen JT, Jørgensen L, Larsen TS, Sorokin A, Bolotin A, Lapidus A, Galleron N, Ehrlich SD and Berka RM. 2004. Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biology 5:r77. https://doi.org/10.1186/gb-2004-5-10-R77

Savluchinske FS, Barbosa A, Cabrita M, Nunes L, Esteves A, Roseiro JC and Curto MJ. 2004. zJournal of Industrial Microbiology and Biotechnology 31:199-203. https://doi.org/10.1007/s10295-004-0133-x

Schallmey M, Singh A and Ward OP. 2004. Developments in the use of Bacillus species for industrial production. Canadian Journal of Microbiology 50:1-17. https://doi.org/10.1139/w03-076

Selim S, Negrel J, Govaerts C, Gianinazzi S and Van Tuinen D. 2005 Isolation and partial characterization of antagonistic peptides produced by Paenibacillus sp. strain B2 isolated from the sorghum mycorrhizosphere. Applied and Environmental Microbiology 71:6501-6507. https://doi.org/10.1128/AEM.71.11.6501-6507.2005

Shelburne CE, An FY, Dholpe V, Ramamoorthy A, Lopatin DE and Lantz MS. 2007. The spectrum of antimicrobial activity of the bacteriocin subtilosin A. Journal of Antimicrobial Chemotherapy 59:297-300. https://doi.org/10.1093/jac/dkl495

Slater J. 1985. Microbial growth dynamics. In: Comprehensive biotechnology, Mac-Young, M. (eds). Oxforf Pergamosm, p. 184-213.

Smalla K, Wachtendorf U, Hever H, Liu WT and Forney L. 1998. Analysis of BIOLOG GN substrate utilization patterns by microbial communities. Applied and Environmental Microbiology 64:1220-1225. Disponible en línea: http://aem.asm.org/content/64/4/1220.short

Stein T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Molecular Microbiology 56:845-857. https://doi.org/10.1111/j.1365-2958.2005.04587.x

Tamehiro N, Okamoto-Hosoya Y, Okamoto S, Ubukata M, Hamada M, Naganawa H and Ochi K. 2002. Bacilysocin, a novel phospholipid antibiotic produced by Bacillus subtilis 168. Antimicrobial Agents and Chemotherapy 46:315-320. https://doi.org/10.1128/AAC.46.2.315-320.2002

Vandenhove H, Merck R, Van Steenbergen M and Vlassak K. 1993. Microcalorimetric characterization, physiological stages and survival ability of Azospirillum brasilense. Soil Biology and Biochemistry 25:513-519. https://doi.org/10.1016/0038-0717(93)90077-O

Veith B, Herzberg C, Steckel S, Feesche J, Maurer KH, Ehrenreich P, Bäumer S, Henne A, Liesegang H, Merkl R, Ehrenreich A and Gottschalk G. 2004. The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. Journal of Molecular Microbiology and Biotechnology 7:204-211. https://doi.org/10.1159/000079829

Vos P, Hoger R, Bleker M, Reijans M, Van de Lec T, Hones M, Frijters A, Pot J, Peleman J, Kaiper M and Zabeau M. 1995. AFLP: A new technique for DNA fingerprinting. Nucleic Acid Research 23:4407-4414. https://doi.org/10.1093/nar/23.21.4407

Zhang X, Zhanng B, Zhang Z, Shen W, Yang C, Yu J and Zhao Y. 2005. Survival of the biocontrol agents Brevibacillus brevis ZJY-1 and Bacillus subtilis ZJY-116 on the spikes of barley in the field. Journal Zhejiang University SCIENCE. B. 6:770-777. https://doi.org/10.1631/jzus.2005.B0770




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.1711-3

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