Multicellular behaviour and production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent

• Autorzy: Nagorska K. , Bikowski M. , Obuchowski M.
• Języki publikacji: EN

Abstrakty

EN

Intensive cultivation of plants in the monoculture field system in order to feed the continuously growing human population creates a need for their protection from the variety of natural competitors such as: bacteria, fungi, insects as well as other plants. The increase in the use of chemical substances in the 20th century has brought many effective solutions for the agriculture. However, it was extremely difficult to obtain a substance, which would be directed solely against a specific plant pathogen and would not be harmful for the environment. In the late 1900's scientists began trying to use natural antagonisms between resident soil organism to protect plants. This phenomenon was named biocontrol. Biological control of plants by microorganisms is a very promising alternative to an extended use of pesticides, which are often expensive and accumulate in plants or soil, having adverse effects on humans. Nonpathogenic soil bacteria living in association with roots of higher plants enhance their adaptive potential and, moreover, they can be beneficial for their growth. Here, we present the current status of the use of Bacillus subtilis in biocontrol. This prevalent inhabitant of soil is widely recognized as a powerful biocontrol agent. Naturally present in the immediate vicinity of plant roots, B. subtilis is able to maintain stable contact with higher plants and promote their growth. In addition, due to its broad host range, its ability to form endospores and produce different biologically active compounds with a broad spectrum of activity, B. subtilis as well as other Bacilli are potentially useful as biocontrol agents.

Słowa kluczowe

EN

solution; monoculture field system; antimicrobial agent; toxic substance; agriculture; chemical substance; Bacillus subtilis; fungi; plant cultivation; multicellular behaviour; insect; biological control agent; protection; bacteria; biological control

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2007
• Tom: 54
• Numer: 3
• Opis fizyczny: p.495-508,fig.,ref.

Twórcy

autor

Nagorska K.

• University of Gdansk, Debinki 1, 80-211 Gdansk, Poland

autor

Bikowski M.

autor

Obuchowski M.

Bibliografia

• Adebanjo A, Bankole SA (2004) Evaluation of some fungi and bacteria for biocontrol of anthracnose disease of cowpea. J Basic Microbiol 44: 3–9.
• Andersen JB, Koch B, Nielsen TH, Sorensen D, Hansen M, Nybroe O, Christophersen C, Sorensen J, Molin S, Givskov M (2003) Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology 149: 37–46.
• Antelmann H, Towe S, Albrecht D, Hecker M (2007) The phosphorus source phytate changes the composition of the cell wall proteome in Bacillus subtilis. J Proteome Res 6: 897–903.
• Bacon CW, Yates IE, Hinton DM, Meredith F (2001) Biological control of Fusarium moniliforme in maize. Environ Health Perspect 109: 325–332.
• 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 Physiol 134: 307–319.
• Bees MA, Andresen P, Mosekilde E, Givskov M (2000) The interaction of thin-film flow, bacterial swarming and cell differentiation in colonies of Serratia liquefaciens. J Math Biol 40: 27–63.
• Benhamou N, Kloepper JW, Quadt-Hallman A, Tuzun S (1996) Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol 112: 919–929.
• Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and nonmycorrhizal carrot roots. Mol Plant Microbe Interact 14: 255–260.
• Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98: 11621–11626.
• Calvio C, Celandroni F, Ghelardi E, Amati G, Salvetti S, Ceciliani F, Galizzi A, Senesi S (2005) Swarming differentiation and swimming motility in Bacillus subtilis are controlled by swrA, a newly identified dicistronic operon. J Bacteriol 187: 5356–5366.
• Carrillo C, Teruel JA, Aranda FJ, Ortiz A (2003) Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim Biophys Acta Biomembr 1611: 91–97.
• Cavaglieri L, Passone A, Etcheverry M (2004) Screening procedures for selecting rhizobacteria with biocontrol effects upon Fusarium verticillioides growth and fumonisin B1 production. Res Microbiol 155: 747–754.
• Cavaglieri L, Orlando J, Etcheverry M (2005) In vitro influence of bacterial mixtures on Fusarium verticillioides growth and fumonisin B1 production: effect of seeds treatment on maize root colonization. Lett Appl Microbiol 41: 390–396.
• Chen WL, Gong HF, Lin FC, Xu JP, Li DB (1997) The antagonistic activities of Bacillus subtilis A30 to rice pathogens. J Zhejiang Agricul Univ 23: 649–654.
• Connelly MB, Young GM, Sloma A (2004) Extracellular proteolytic activity plays a central role in swarming motility in Bacillus subtilis. J Bacteriol 186: 4159–4167.
• Cosby WM, Vollenbroich D, Lee OH, 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 control. J Bacteriol 180: 1438–1445.
• Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61: 401–422.
• El-Ghaouth A (1997) Biologically-based alternatives to synthetic fungicides for the control of postharvest diseases. J Ind Microbiol Biotechnol 19: 160–162.
• Finking R, Marahiel MA (2004) Biosynthesis of nonribosomal peptides 1. Annu Rev Microbiol 58: 453–488.
• Földes T, Bánhegyi I, Herpai Z, Varga L, Szigeti J (2000) Isolation of Bacillus strains from the rhizosphere of cereals and in vitro screening for antagonism against phytopathogenic, food-borne pathogenic and spoilage micro-organisms. J Appl Microbiol 89: 840–846.
• Grangemard I, Peypoux F, Wallach J, Das BC, Labbe H, Caille A, Genest M, Maget-Dana R, Ptak M, Bonmatin JM (1997) Lipopeptides with improved properties: structure by NMR, purification by HPLC and structureactivity relationships of new isoleucyl-rich surfactins. J Pept Sci 3: 145–154.
• Greiner R, Haller E, Konietzny U, Jany KD (1997) Purification and characterization of a phytase from Klebsiella terrigena. Arch Biochem Biophys 341: 201–206.
• Heerklotz H, Seelig J (2007) Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur Biophys J 36: 305–314.
• Hiradate S, Yoshida S, Sugie H, Yada H, Fujii Y (2002) Mulberry anthracnose antagonists (iturins) produced by Bacillus amyloliquefaciens RC-2. Phytochemistry 61: 693–698.
• Hou X, Boyetchko SM, Brkic M, Olson D, Ross A, Hegedus D (2006) Characterization of the anti-fungal activity of a Bacillus spp. associated with sclerotia from Sclerotinia sclerotiorum. Appl Microbiol Biotechnol 72: 644–653.
• Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148: 2097–2109.
• Izquierdo L, Abitiu N, Coderch N, Hita B, Merino S, Gavin R, Tomás JM, Regué M (2002) The inner-core lipopolysaccharide biosynthetic waaE gene: function and genetic distribution among some Enterobacteriaceae. Microbiology 148: 3485–3496.
• Jeleń F, Oleksy A, Smietana K, Otlewski J (2003) PDZ domains— common players in the cell signaling. Acta Biochim Polon 50: 985–1017.
• Julkowska D, Obuchowski M, Holland IB, Seror SJ (2004) Branched swarming patterns on a synthetic medium formed by wild-type Bacillus subtilis strain 3610: detection of different cellular morphologies and constellations of cells as the complex architecture develops. Microbiology 150: 1839–1849.
• Julkowska D, Obuchowski M, Holland IB, Seror SJ (2005) Comparative analysis of the development of swarming communities of Bacillus subtilis 168 and a natural wild type: critical effects of surfactin and the composition of the medium. J Bacteriol 187: 65–76.
• Kawulka KE, Sprules T, Diaper CM, Whittal RM, McKay RT, Mercier P, Zuber P, Vederas JC (2004) Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to alpha-carbon crosslinks: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry 43: 3385–3395.
• Kearns DB, Losick R (2003) Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 49: 581–590.
• Kearns DB, Chu F, Rudner R, Losick R (2004) Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol Microbiol 52: 357–369.
• Kerovuo J, Lauraeus M, Nurminen P, Kalkkinen N, Apajalahti J (1998) Isolation, characterization, molecular gene cloning, and sequencing of a novel phytase from Bacillus subtilis. Appl Environ Microbiol 64: 2079–2085.
• Kim YO, Lee JK, Kim HK, Yu JH, Oh TK (1998) Cloning of the thermostable phytase gene (phy) from Bacillus sp. DS11 and its overexpression in Escherichia coli. FEMS Microbiol Lett 162: 185–191.
• Kim PI, Chung KC (2004) Production of an antifungal protein for control of Colletotrichum lagenarium by Bacillus amyloliquefaciens MET0908. FEMS Microbiol Lett 234: 177–183.
• Kinsinger RF, Shirk MC, Fall R (2003) Rapid surface motility in Bacillus subtilis is dependent on extracellular surfactin and potassium ion. J Bacteriol 185: 5627–5631.
• Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286: 885–886.
• Kowall M, Vater J, Kluge B, Stein T, Franke P, Ziessow D (1998) Separation and characterization of surfactin isoforms produced by Bacillus subtilis OKB 105 J Colloid Interface Sci 204: 1–8.
• Kraus J, Loper JE (1995) Characterization of a genomic region required for production of the antibiotic pyoluteorin by the biological control agent Pseudomonas fluorescens Pf-5. Appl Environ Microbiol 61: 849–854.
• Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Danchin A (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249–256.
• Leclere V, Bechet M, Adam A, Guez JS, Wathelet B, Ongena M, Thonart P, Gancel F, Chollet-Imbert M, Jacques P (2005) Mycosubtilin overproduction by Bacillus subtilis
• BBG100 enhances the organism’s antagonistic and biocontrol activities. Appl Environ Microbiol 71: 4577–4584.
• Leclere V, Marti R, Bechet M, Fickers P, Jacques P (2006) The lipopeptides mycosubtilin and surfactin enhance spreading of Bacillus subtilis strains by their surface-active properties. Arch Microbiol 186: 475–483.
• Leroux P (2003) Modes of action of agrochemicals against plant pathogenic organisms. C R Biol 326: 9–21.
• Lim JH, Park BK, Kim MS, Hwang MH, Rhee MH, Park SC, Yun HI (2005) The anti-thrombotic activity of surfactins. J Vet Sci 6: 353–355.
• Li B, Xie GL, Soad A, Coosemans J (2005) Suppression of Meloidogyne javanica by antagonistic and plant growthpromoting rhizobacteria. J Zhejiang Univ Sci B 6: 496– 501.
• Lin D, Qu LJ, Gu H, Chen Z (2001) A 3.1-kb genomic fragment of Bacillus subtilis encodes the protein inhibiting growth of Xanthomonas oryzae pv. oryzae. J Appl Microbiol 91: 1044–1050.
• Liu JY, Liu W, Pan NS, Chen ZL (1991) The characterization of antagonistic bacterium A014 and its antibacterial protein. Acta Botanica Sinica 33: 157–161.
• Liu J, Liu M, Wang J, Yao JM, Pan RR, Yu ZL (2005) Enhancement of the Gibberella zeae growth inhibitory lipopeptides from a Bacillus subtilis mutant by ion beam implantation. Appl Microbiol Biotechnol 69: 223–228.
• Madhaiyan M, Suresh Reddy BV, Anandham R, Senthilkumar M, Poonguzhali S, Sundaram SP, Sa T (2006) Plant growth-promoting Methylobacterium induces defense responses in groundnut (Arachis hypogaea L.) compared with rot pathogens. Curr Microbiol 53: 270–276.
• Maget-Dana R, Peypoux F (1994) Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87: 151–174.
• Manjula K, Podile AR (2001) Chitin-supplemented formulations improve biocontrol and plant growth promoting efficiency of Bacillus subtilis AF 1. Can J Microbiol 47: 618–625.
• Manjula K, Kishore GK, Podile AR (2004) Whole cells of Bacillus subtilis AF 1 proved more effective than cellfree and chitinase-based formulations in biological control of citrus fruit rot and groundnut rust. Can J Microbiol 50: 737–744.
• Marten P, Smalla K, Berg G (2000) Genotypic and phenotypic differentiation of an antifungal biocontrol strain belonging to Bacillus subtilis. J Appl Microbiol 89: 463–471.
• Matsuyama T, Kaneda K, Nakagawa Y, Isa K, Hara-Hotta H, Yano I (1992) A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and -independent spreading growth of Serratia marcescens. J Bacteriol 74: 1769–1776.
• Maugenest S, Martinez I, Godin B, Perez P, Lescure AM (1999) Structure of two maize phytase genes and their spatio-temporal expression during seedling development. Plant Mol Biol 39: 503–514.
• Mireles JR, Toguchi A, Harshey RM (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183: 5848–5854.
• Mizumoto S, Hirai M, Shoda M (2006) Production of lipopeptide antibiotic iturin A using soybean curd residue cultivated with Bacillus subtilis in solid-state fermentation. Appl Microbiol Biotechnol 72: 869–875.
• Morikawa M (2006) Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J Biosci Bioeng 101: 1–8.
• Moszer I (1998) The complete genome of Bacillus subtilis: from sequence annotation to data management and analysis. FEBS Lett 430: 28–36.
• Mulligan CN (2005) Environmental applications for biosurfactants. Environ Pollut 133: 183–198.
• Munimbazi C, Bullerman LB (1998) Isolation and partial characterization of antifungal metabolites of Bacillus pumilus. J Appl Microbiol 84: 959–968.
• Murudkar CS, Kodgire P, Krishnamurthy Rao K (2006) The carboxy terminal domain of Epr, a minor extracellular serine protease, is essential for the swarming motility of Bacillus subtilis. FEMS Microbiol Lett 257: 24–31.
• Nakano MM, Corbell N, Besson J, Zuber P (1992) Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis. Mol Gen Genet 232: 313–321.
• Naruse N, Tenmyo O, Kobaru S, Kamei H, Miyaki T, Konishi M, Oki T (1990) Pumilacidin, a complex of new antiviral antibiotics. Production, isolation, chemical properties, structure and biological activity. J Antibiot (Tokyo) 43: 267–280.
• Nielsen TH, Sorensen D, Tobiasen C, Andersen JB, Christophersen C, Givskov M, Sorensen J (2002) Antibiotic and biosurfactant properties of cyclic lipopeptides produced by fluorescent Pseudomonas spp. from the sugar beet rhizosphere. Appl Environ Microbiol 68: 3416–3423.
• Okigbo RN (2005) Biological control of postharvest fungal rot of yam (Dioscorea spp.) with Bacillus subtilis. Mycopathologia 159: 307–314.
• Ongena M, Duby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant Microbe Interact 17: 1009–1018.
• Ongena M, Duby F, Jourdan E, Beaudry T, Jadin V, Dommes J, Thonart P (2005a) Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl Microbiol Biotechnol 67: 692–698.
• Ongena M, Jacques P, Toure Y, Destain J, Jabrane A, Thonart P (2005b) Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Appl Microbiol Biotechnol 69: 29–38.
• Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny JL, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9: 1084–1090.
• Pandey A, Palni LM (1997) Bacillus species: the dominant bacteria of the rhizosphere of established tea bushes. Microbiol Res 152: 359–365.
• Park RY, Sun HY, Choi MH, Bai YH, Chung YY, Shin SH (2006) Proteases of a Bacillus subtilis clinical isolate facilitate swarming and siderophore-mediated iron uptake via proteolytic cleavage of transferrin. Biol Pharm Bull 29: 850–853.
• Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51: 553–563.
• Priest FG (1993) Systematics and ecology of Bacillus. In Bacillus subtilis and other gram positive bacteria: biochemistry, physiology, and molecular genetics (Sonenshein AL, Hoch JA, Losick R, eds) pp 3–16. American Society for Microbiology. Washington D.C.
• Przestalski S, Sarapuk J, Kleszczyńska H, Gabrielska J, Hladyszowski J, Trela Z, Kuczera J (2000) Influence of amphiphilic compounds on membranes. Acta Biochim Polon 47: 627–638.
• Raupach GS, Kloepper JW (1998) Mixtures of plant growthpromoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88: 1158–1164.
• Ren D, Sims JJ, Wood TK (2002) Inhibition of biofilm formation and swarming of Bacillus subtilis by (5Z)-4-bromo-5-(bromomethylene)-3–butyl-2(5H)-furanone. Lett Appl Microbiol 34: 293–299.
• Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas spp. that utilize inositol phosphates. Can J Microbiol 43: 509–516.
• Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25: 641–649.
• Romero D, de Vicente A, Rakotoaly RH, Dufour SE, Veening JW, Arrebola E, Cazorla FM, Kuipers OP, Paquot M, Perez-Garcia A (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact 20: 430–440.
• Ron EZ, Rosenberg E (2001) Natural roles of biosurfactants. Environ Microbiol 3: 229–236.
• Shapiro JA (1998) Thinking about bacterial population as multicellular organisms. Annu Rev Microbiol 52: 6308–6321.
• Sieber SA, Marahiel MA (2003) Learning from nature’s drug factories: nonribosomal synthesis of macrocyclic peptides. J Bacteriol 185: 7036–7043.
• Singh P, Cameotra SS (2004) Potential applications of microbial surfactants in biomedical sciences. Trends Biotechnol 22: 142–146.
• Sharga BM, Lyon GD (1998) Bacillus subtilis BS 107 as an antagonist of potato blackleg and soft rot bacteria. Can J Microbiol 44: 777–783.
• Souto GI, Correa OS, Montecchia MS, Kerber NL, Pucheu NL, Bachur M, Garcia AF (2004) Genetic and functional characterization of a Bacillus sp. strain excreting surfactin and antifungal metabolites partially identified as iturin-like compounds. J Appl Microbiol 97: 1247–1256.
• Stein T, Borchert S, Conrad B, Feesche J, Hofemeister B, Hofemeister J, Entian KD (2002) Two different antibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3. J Bacteriol 184: 1703–1711.
• Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56: 845–857.
• Stover AG, Driks A (1999) Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. J Bacteriol 181: 1664–1672.
• Symmank H, Franke P, Saenger W, Bernhard F (2002) Modification of biologically active peptides: production of a novel lipohexapeptide after engineering of Bacillus subtilis surfactin synthetase. Protein Eng 15: 913–921.
• Thennarasu S, Lee DK, Poon A, Kawulka KE, Vederas JC, Ramamoorthy A (2005) Membrane permeabilization, orientation, and antimicrobial mechanism of subtilosin A. Chem Phys Lipids 137: 38–51.
• Thimon L, Peypoux F, Maget-Dana R, Roux B, Michel G (1992) Interactions of bioactive lipopeptides, iturin A and surfactin from Bacillus subtilis. Biotechnol Appl Biochem 16: 144–151.
• Thimon L, Peypoux F, Exbrayat JM, Michel G (1994) Effect of iturin A, a lipopeptide from Bacillus subtilis on morphology and ultrastructure of human erythrocytes. Cytobios 79: 69–83.
• Timmusk S, Grantcharova N, Wagner EG (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71: 7292–7300.
• Toguchi A, Siano M, Burkart M, Harshey RM (2000) Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J Bacteriol 182: 6308–6321.
• Toure Y, Ongena M, Jacques P, Guiro A, Thonart P (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96: 1151–1160.
• Tsuge K, Ano T, Hirai M, Nakamura Y, Shoda M (1999) The genes degQ, pps, and lpa-8 (sfp) are responsible for conversion of Bacillus subtilis 168 to plipastatin production. Antimicrob Agents Chemother 43: 2183–2192.
• Tsuge K, Inoue S, Ano T, Itaya M, Shoda M (2005) Horizontal transfer of iturin A operon, itu, to Bacillus subtilis 168 and conversion into an iturin A producer. Antimicrob Agents Chemother 49: 4641–4648.
• Tye AJ, Siu FK, Leung TY, Lim BL (2002) Molecular cloning and the biochemical characterization of two novel phytases from Bacillus subtilis 168 and Bacillus licheniformis. Appl Microbiol Biotechnol 59: 190–197.
• Van Loon LC, Bakker PAHM, Pietrase CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36: 453–483.
• Vullo DL, Coto CE, Siñeriz F (1991) Characteristics of an inulinase produced by Bacillus subtilis 430A, a strain isolated from the rhizosphere of Vernonia herbacea (Vell Rusby). Appl Environ Microbiol 57: 2392–2394.
• Walker R, Ferguson CMJ, Booth NA, Allan EJ (2002) The symbiosis of Bacillus subtilis L-forms with Chinese cabbage seedlings inhibits conidial germination of Botrytis cinerea. Lett Appl Microbiol 34: 42–45.
• Wyss M, Brugger R, Kronenberger A, Rémy R, Fimbel R, Oesterhelt G, Lehmann M, van Loon AP (1999) Biochemical characterization of fungal phytases (myo-inositol hexakisphosphate phosphohydrolases): catalytic properties. Appl Environ Microbiol 65: 367–373.
• Yakimov MM, Fredrickson HL, Timmis KN (1996) Effect of heterogeneity of hydrophobic moieties on surface activity of lichenysin A, a lipopeptide biosurfactant from Bacillus licheniformis BAS50. Biotechnol Appl Biochem 23: 13–18.
• Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL (2002) Production of iturin A by Bacillus amyloliquefaciens supressing Rhizoctonia solani. Soil Biol Biochem 34: 955–963.
• Zhang X, Zhang BX, Zhang Z, Shen WF, Yang CH, Yu JQ, Zhao YH (2005) Survival of the biocontrol agents Brevibacillus brevis ZJY-1 and Bacillus subtilis ZJY-116 on the spikes of barley in the field. J Zhejiang Univ Sci B 6: 770–777.
• Zhao JZ, Cao J, Collins HL, Bates SL, Roush RT, Earle ED, Shelton AM (2005) Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc Natl Acad Sci USA 102: 8426–8430.