Natural products from Bacillus subtilis with antimicrobial properties

doi:10.1016/j.cjche.2014.05.020

Chin.J.Chem.Eng. ›› 2015, Vol. 23 ›› Issue (4): 744-754.DOI: 10.1016/j.cjche.2014.05.020

Natural products from Bacillus subtilis with antimicrobial properties

Tao Wang^1,2, Yafei Liang^1,3, Mianbin Wu^1,2,4, Zhengjie Chen⁴, Jianping Lin^1,2, Lirong Yang^1,2

1 Key Laboratory of Biomass Chemical Engineering of Ministry of Education, Hangzhou 310027, China;
2 Department of Chemical and Biological Engineering, Zhejiang University, Hangzhou 310027, China;
3 JinhuaPeople's Hospital, Jinhua 321000, China;
4 Zhejiang Key Laboratory of Antifungal Drugs, Taizhou 318000, China

Received:2013-10-10 Revised:2014-05-15 Online:2015-05-13 Published:2015-04-28
Contact: Mianbin Wu
Supported by:
Supported by theNationalNatural Science Foundation of China (21376215),the National Science and Technology Major Project of New Drug,China (2012ZX09103101-075),the Innovative Research Platform co-constructed by Zhejiang University and Taizhou City,and the Science and Technology Project of Zhejiang Province (2014C33174),the Major State Basic Research Development Program of China (2011CB710803),and the National High-Tech Research and Development Program of China (2012AA022302).

Natural products from Bacillus subtilis with antimicrobial properties

Tao Wang^1,2, Yafei Liang^1,3, Mianbin Wu^1,2,4, Zhengjie Chen⁴, Jianping Lin^1,2, Lirong Yang^1,2

1 Key Laboratory of Biomass Chemical Engineering of Ministry of Education, Hangzhou 310027, China;
2 Department of Chemical and Biological Engineering, Zhejiang University, Hangzhou 310027, China;
3 JinhuaPeople's Hospital, Jinhua 321000, China;
4 Zhejiang Key Laboratory of Antifungal Drugs, Taizhou 318000, China

通讯作者: Mianbin Wu
基金资助:
Supported by theNationalNatural Science Foundation of China (21376215),the National Science and Technology Major Project of New Drug,China (2012ZX09103101-075),the Innovative Research Platform co-constructed by Zhejiang University and Taizhou City,and the Science and Technology Project of Zhejiang Province (2014C33174),the Major State Basic Research Development Program of China (2011CB710803),and the National High-Tech Research and Development Program of China (2012AA022302).

Abstract

Abstract: Bacillus subtilis produces many chemically-diverse secondary metabolites of interest to chemists and biologists. Based on this, this review gives a detailed overview of the natural components produced by B. subtilis including cyclic lipopeptides, polypeptides, proteins (enzymes), and non-peptide products. Their structures, bioactive activities and the relevant variants as novel lead structures for drug discovery are also described. The challenging effects of fermentation metabolites, isolation and purification, as well as the overproduction of bioactive compounds from B. subtilis by metabolic engineering, were also highlighted. Systematically exploring biosynthetic routes and the functions of secondary metabolites from B. subtilis may not only be beneficial in improving yields of the products, but also in helping themto be used in food industry and publicmedical service on a large-scale.

Key words: Bacillus subtilis, Antimicrobial, Bioseparation, Drug design

摘要： Bacillus subtilis produces many chemically-diverse secondary metabolites of interest to chemists and biologists. Based on this, this review gives a detailed overview of the natural components produced by B. subtilis including cyclic lipopeptides, polypeptides, proteins (enzymes), and non-peptide products. Their structures, bioactive activities and the relevant variants as novel lead structures for drug discovery are also described. The challenging effects of fermentation metabolites, isolation and purification, as well as the overproduction of bioactive compounds from B. subtilis by metabolic engineering, were also highlighted. Systematically exploring biosynthetic routes and the functions of secondary metabolites from B. subtilis may not only be beneficial in improving yields of the products, but also in helping themto be used in food industry and publicmedical service on a large-scale.

关键词: Bacillus subtilis, Antimicrobial, Bioseparation, Drug design

Tao Wang, Yafei Liang, Mianbin Wu, Zhengjie Chen, Jianping Lin, Lirong Yang. Natural products from Bacillus subtilis with antimicrobial properties[J]. Chin.J.Chem.Eng., 2015, 23(4): 744-754.

Tao Wang, Yafei Liang, Mianbin Wu, Zhengjie Chen, Jianping Lin, Lirong Yang. Natural products from Bacillus subtilis with antimicrobial properties[J]. Chinese Journal of Chemical Engineering, 2015, 23(4): 744-754.

References

[1] P. Coates, S. Vyakrnam, E.A. Eady, C.E. Jones, J.H. Cove, W.J. Cunliffe, Prevalence of antibiotic-resistant propionibacteria on the skin of acne patients: 10-year surveillance data and snapshot distribution study, Brit. J. Dermatol. 146 (2002) 840-848.

[2] S.K. Field, D. Fisher, J.M. Jarand, R.L. Cowie, New treatment options for multidrugresistant tuberculosis, Ther. Adv. Respir. Dis. 6 (5) (2012) 255-268.

[3] C.R. Harwood, Bacillus subtilis and its relatives: Molecular biological and industrial workhorses, Trends Biotechnol. 10 (1992) 247-256.

[4] S.Mukherj, P. Das, R. Sen, Towards commercial production ofmicrobial surfactants, Trends Biotechnol. 24 (11) (2006) 509-515.

[5] C.N. Mulligan, Environmental applications for biosurfactants, Environ. Pollut. 133 (2) (2005) 183-198.

[6] G.A.L. Broggini, B. Duffy, E. Holliger, H.J. Schärer, C. Gessler, A. Patocchi, Detection of the fire blight biocontrol agent Bacillus subtilis BD170 (Biopro) in a Swiss apple orchard, Eur. J. Plant Pathol. 111 (2005) 93-100.

[7] L. Serrano, D. Manker, F. Brandi, T. Cali, The use of Bacillus subtilis QST 713 and Bacillus pumilus QST 2808 as protectant fungicides in conventional application programs for black leaf streak control, Acta Horticult. (ISHS) 986 (2013) 149-155.

[8] R.G. Linderman, C.J. Masters, E.A. Davis, Efficacy of chemical and biological agents to suppress fusarium and pythium damping-off of container-grown Douglas-fir seedlings, Plant Health Prog. (2008). http://dx.doi.org/10.1094/PHP-2008-0317- 02-RS.

[9] X.L. Lu, Q.Z. Xua, X.Y. Liu, X. Cao, K.Y. Ni, B.H. Jiao, Marine drugs — macrolactins, Chem. Biodivers. 5 (2008) 1669-1674.

[10] M. Ongena, P. Jacques, M. Ongena, P. Jacques, Bacillus lipopeptides: Versatile weapons for plant disease biocontrol, Trends Microbiol. 16 (3) (2008) 115-125.

[11] F. Besson, F. Peypoux, G.Michel, L. Delcambe, Characterization of iturin A in antibiotics from various strains of Bacillus subtilis, J. Antibiot. 29 (10) (1976) 1043-1049.

[12] M.A. Klich, K.S. Arthur, A.R. Lax, J.M. Bland, Iturin A: A potential new fungicide for stored grains, Mycopathologia 127 (1994) 123-127.

[13] S.J. Cho, S.K. Lee, B.J. Cha, Y.H. Kim, K.S. Shin, Detection and characterization of the Gloeosporium gloeosporioides growth inhibitory compound iturin A from Bacillus subtilisstrain KS03, FEMS Microbiol. Lett. 223 (1) (2003) 47-51.

[14] L. Volpon, F. Besson, J.M. Lancelin, NMR structure of active and inactive forms of the sterol-dependent antifungal antibiotic bacillomycin L, Eur. J. Biochem. 264 (1999) 200-210.

[15] N. Roongsawang, J. Thaniyavarn, S. Thaniyavarn, T. Kameyama, M. Haruki, T. Imanaka, M. Morikawa, S. Kanaya, Isolation and characterization of a halotolerant Bacillus subtilis BBK-1 which produces three kinds of lipopeptides: Bacillomycin L, plipastatin, and surfactin, Extremophiles 6 (6) (2002) 499-506.

[16] R.B. Walton, H.B. Woodruff, A crystalline antifungal agent, mycosubtilin, isolated from sulbtilin broth, J. Antibiot. 39 (1996) 636-641.

[17] M.L. Hourdou, F. Besson, I. Tenoux, G. Michel, Fatty acid and β-amino acid syntheses in strains of Bacillus subtilis producing iturinic antibiotics, Lipides 1123 (1) (1992) 51-58.

[18] C.G. Phae, M. Shoda, H. Kubota, Suppressive effect of Bacillus subtilis and it's products on phytopathogenic microorganisms, J. Ferment. Bioeng. 69 (1) (1990) 1-7.

[19] Y.F. Ye, Q.Q. Li, F.U. Gang, G.Q. Yuan, J.H. Miao, W. Lin, Identification of antifungal substance (Iturin A2) produced by Bacillus subtilis B47 and its effect on southern corn leaf blight, J. I. A. 11 (1) (2012) 90-99.

[20] I.G.F. Peypoux, H. Labbe, J. Wallach, B.C. Das, H. Labbé, A. Caille, M. Genest, R. Maget-Dana, M. Ptak, J.M. Bonmatin, Lipopeptides with improved properties: Structure by NMR, purification by HPLC and structure-activity relationships of new isoleucyl-rich surfactins, J. Pept. Sci. 3 (1997) 145-154.

[21] G.Y. Yu, J.B. Siclair, G.L. Hartman, B. Bertagnolli, Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani, Soil Biol. Biochem. 34 (2002) 955-963.

[22] H. Syuntaro, S. Yoshida,Which quite differs fromthemembers of the iturins family that are restricted to bacillus subtilis, Phytochemistry (2002) 693-698.

[23] A.L. Moyne, R. Shelby, T.E. Cleveland, S. Tuzun, Bacillomycin D: An iturin with antifungal activity against Aspergillus flavus, J. Appl. Microbiol. 90 (2001) 622-629.

[24] F. Besson, G. Michel, Isolation and characterization of new iturin D and iturin E, J. Antibiot. 40 (4) (1986) 437-442.

[25] O. Asaka,M. Shoda, Biocontrol of Rhizoctonia solani damping-off of tomatowith Bacillus subtilis RB14, Appl. Environ. Microbiol. 62 (1986) 4081-4085.

[26] A.S. Kumar, S. Saini, V. Wray,M. Nimtz, A. Prakash, B.N. Johri, Characterization of an antifungal compound produced by Bacillus sp. strain A(5) F that inhibits Sclerotinia sclerotiorum, J. Basic Microbiol. 52 (6) (2012) 670-678.

[27] M.A. Klich, A.R. Lax, J.M. Bland, Inhibition of some mycotoxigenic fungi by iturin A, a peptidolipid produced by Bacillus subtilis, Mycopathologia 116 (1991) 77-80.

[28] W. Loeffler, J.S.M. Tschen,N.Vanittanakom,M. Kugler, E.Knorpp, T.F.Hsieh,M. S., T.G. Wu, Antifungal effects of bacilysin and fengymycin from Bacillus suhtilis F-29-3 A comparisonwith activities of other Bacillus antibiotics, J. Phytopathol. 115 (1986) 204-213.

[29] M. Szczech, M. Shoda, The effect of mode of application of Bacillus subtilis RB14-C on its efficacy as a biocontrol agent against Rhizoctonia solani, J. Phytopathol. 154 (2006) 370-377.

[30] S. Mizumoto, M. Hirai, M. Shoda, Enhanced iturin A production by Bacillus subtilis and its effect on suppression of the plant pathogen Rhizoctonia solani, Appl. Microbiol. Biotechnol. 75 (6) (2007) 1267-1274.

[31] E. Montesinos, Development, registration and commercialization of microbial pesticides for plant protection, Int Microbiol. 6 (4) (2003) 245-252.

[32] J.M. Raaijmakers, B.I. De, O. Nybroe, M. Ongena, Natural functions of lipopeptides from Bacillus and Pseudomonas: More than surfactants and antibiotics, FEMS Microbiol. Rev. 34 (6) (2010) 1037-1062.

[33] W. Liu, X. Wang, L. Wu, M. Chen, C. Tu, Y. Luo, P. Christie, Isolation, identification and characterization of Bacillus amyloliquefaciens BZ-6, a bacterial isolate for enhancing oil recovery from oily sludge, Chemosphere 87 (10) (2012) 1105-1110.

[34] B. Yuan, Z. Wang, S. Qin, G.H. Zhao, Y.J. Feng, L.H. Wei, J.H. Jiang, Study of the antisapstain fungus activity of Bacillus amyloliquefaciens CGMCC 5569 associated with Ginkgo biloba and identification of its active components, Bioresour. Technol. 114 (2012) 536-541.

[35] P.I. Kim, H. Bai, D. Bai, D. Chae, S. Chung, Y. Kim, R. Park, Y.T. Chi, Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26, J. Appl. Microbiol. 97 (5) (2004) 942-949.

[36] T.P. Lin, C.L. Chen, C.H. Fu, C.Y. Wu, G.H. Lin, S.H. Huang, L.K. Chang, S.T. Liu, Functional analysis of fengycin synthetase FenD, Biochim. Biophys. Acta 1730 (2) (2005) 159-164.

[37] S. Steller,D. Vollenbroich, F. Leenders, T. Stein, B. Conrad, J.Hofemeister, P. Jacques, P. Thonart, J. Vater, Structural and functional organization of the fengycin synthetase multienzyme system from Bacillus subtilis b213 and A173, Chem. Biol. 6 (1999) 31-41.

[38] M. Ongena, P. Jacques, Y. Touré, J. Destain, A. Jabrane, P. Thonart, Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis, Appl. Microbiol. Biotechnol. 69 (1) (2005) 29-38.

[39] Yánez-Mendizábal, V. Viñas, I. Usall, J.R. Torres, C. Solsona, M. Abadias, N. Teixidó, Production of the postharvest biocontrol agent Bacillus subtilis CPA-8 using low cost commercial products and by-products, J. Appl.Microbiol. 60 (3) (2012) 280-289.

[40] D. Romero, E. Arrebola, R.H. Rakotoaly, S.E. Dufour, J.W. Veening, E. Arrebola, F.M. Cazorla, O.P. Kuipers, M. Paquot, A. Pérez-García, The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward podosphaera fusca, Mol. Plant Microbe Interact. 20 (4) (2006) 430-440.

[41] F. Peypoux, J.M. Bonmatin, J. Wallach, Recent trends in the biochemistry of surfactin, Appl. Microbiol. Biotechnol. 51 (1999) 553-563.

[42] N.I. Kalinovskaya, T.A. Kuznetsova, Y.V. Rashkes, M.Y. Mil'grom, E.G. Mil'grom, R.H. Willis, A.I.Wood, H.A. Kurtz, C. Carabedian, P. Murphy, G.B. Elyakov, Surfactin-like structures of five cyclic depsipeptides from the marine isolate of Bacillus pumilus, Russ. Chem. B+ 44 (5) (1995) 951-954.

[43] A. Savadogo, A. Tapi, M. Chollet, B.Wathelet, A.S. Traoré, P.h. Jacques, Identification of surfactin producing strains in Soumbala and Bikalga fermented condiments using Polymerase Chain Reaction and Matrix Assisted Laser Desorption/Ionization- Mass Spectrometry methods, Int. J. Food Microbiol. 151 (3) (2001) 299-306.

[44] J.M. Bonmatin, H. Labbé, I. Grangemard, F. Peypoux, R. Maget-Dana, M. Ptak, l G. Miche, Production, isolation and characterization of [Leu4]- and [Ile4]surfactins from Bacillus subtilis, Lett. Pept. Sci. 2 (1995) 41-47.

[45] S. Nakayama, S. Takahashi,M. Hirai,M. Shoda, Isolation of new variants of surfactin by a recombinant Bacillus subtilis, Appl. Microbiol. Biotechnol. 48 (1997) 80-82.

[46] A.F. de Faria, D.S. Teodoro-Martinez, G.N. de Oliveira Barbosa, Production and structural characterization of surfactin (C14/Leu7) produced by Bacillus subtilis isolate LSFM-05 grown on raw glycerol from the biodiesel industry, Process Biochem. 46 (10) (2001) 1951-1957.

[47] P. Singh, S.S. Cameotra, Potential applications of microbial surfactants in biomedical sciences, Trends Biotechnol. 22 (3) (2004) 142-146.

[48] R.S. Makkar, S.S. Cameotra, An update on the use of unconventional substrates for biosurfactant production and their new applications, Appl. Microbiol. Biotechnol. 58 (4) (2002) 428-434.

[49] H. Razafindralambo, Y. Popineau, M. Deleu, C. Hbid, P. Jacques, P. Thonart,M. Paquot, Foaming properties of lipopeptides produced by Bacillus subtilis: effect of lipid and peptide structural attributes, J. Agric. Food Chem. 46 (1998) 911-916.

[50] D. Vollenbroich,M. Ozel, J. Vater, R.M. Kamp, G. Pauli,Mechanism of inactivation of enveloped viruses by the biosurfactant surfactin fromBacillus subtilis, Biologicals 25 (1997) 289-297.

[51] M. Kracht, H. Rokos, M. Ozel, M. Kowall, G. Pauli, J. Vater, Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives, J. Antibiot. 52 (7) (1999) 613-619.

[52] F. Rivardo, M.G. Martinotti, R.J. Turner, H. Ceri, Synergistic effect of lipopeptide biosurfactant with antibiotics against Escherichia coli CFT073 biofilm, Int. J. Antimicrob. Agents 37 (4) (2011) 324-331.

[53] R.V. Velho, L.F. Medina, J. Segalin, A. Brandelli, Production of lipopeptides among Bacillus strains showing growth inhibition of phytopathogenic fungi, Folia Microbiol. 56 (4) (2011) 297-303.

[54] D. Ghribi,M. Elleuch, L. Abdelkefi, S. Ellouze-Chaabouni, Evaluation of larvicidal potency of Bacillus subtilis SPB1 biosurfactant against Ephestia kuehniella (Lepidoptera: Pyralidae) larvae and influence of abiotic factors on its insecticidal activity, J. Stored Prod. Res. 48 (2012) 68-72.

[55] D.C. Sabaté, L. Carrillo, M.C. Audisio, Inhibition of Paenibacillus larvae and Ascosphaera apis by Bacillus subtilis isolated from honeybee gut and honey samples, Res. Microbiol. 160 (2009) 193-199.

[56] G. Hagelin, I. Oulie, A. Raknes, K. Undheim, O.G. Clausen, Preparative highperformance liquid chromatographic separation and analysis of the maltacine complex — a family of cyclic peptide antibiotics fromBacillus subtilis, J. Chromatogr. B 811 (2) (2004) 243-251.

[57] G. Hagelin, B. Indrevoll, H.J. Thomas, Use of synthetic analogues in confirmation of structure of the peptide antibiotics maltacines, Int. J. Mass Spectrom. 268 (2-3) (2007) 254-264.

[58] J.E. Walker, E.P. Abaraham, Isolation of bacilysin and a newamino acid fromculture filtrates of Bacillus subtilis, Biochem. J. 118 (1970) 557-561.

[59] J.E.Walker, E.P. Abaraham, The structure of bacilysin and other products of Bacillus subtilis, Biochem. J. 118 (1970) 563-570.

[60] M. Kenig, E. Vandamme, E.P. Abraham, The mode of action of bacilysin and anticapsin and biochemical properties of bacilysin-resistant mutants, J. Gen. Microbiol. 94 (1976) 46-54.

[61] J.B. Parker, C.T. Walsh, Stereochemical outcome at four stereogenic centers during conversion of prephenate to tetrahydrotyrosine by BacABGF in the bacilysin pathway, Biochemistry 51 (28) (2012) 5622-5632.

[62] M. Kenig, P.E. Abraham, Antimicrobial activities and antagonists of bacilysin and anticapsin, J. Gen. Microbiol. 94 (1976) 37-45.

[63] C. Rapp, G. Jung, M. Kugler, W. Loeffler, Rhizocticins — New phosphonooligopeptides with antifungal activity, Eur. J. Org. Chem. 7 (1988) 655-661.

[64] M. Kugler, W. Loeffier, C. Rapp, A. Kern, G. Jung, Rhizocticin A, an antifungal phosphono-oligopeptide of Bacillus subtilis ATCC 6633: Biological properties, Arch. Microbiol. 153 (1990) 276-281.

[65] K. Kino, Y. Kotanaka, T. Arai, M. Yagasaki, A novel L-amino acid ligase from Bacillus subtilis NBRC3134, a microorganism producing peptide-antibiotic rhizocticin, Biosci. Biotechnol. Biochem. 73 (4) (2009) 901-907.

[66] S.A. Borisova, B.T. Circello, J.K. Zhang,W.A. van der Donk,W.W. Metcalf, Biosynthesis of rhizocticins, antifungal phosphonate oligopeptides produced by Bacillus subtilis ATCC6633, Chem. Biol. 17 (1) (2010) 28-37.

[67] J. Itoh, S. Omoto, T. Shomura, Amicoumacin: A new antibiotic with strong antiinflammatory and antiulcer activity, J. Antibiot. 34 (5) (1980) 611-613.

[68] Y. Li, Y. Xu, L. Liu, Z. Han, P.Y. Lai, X. Guo, X. Zhang, W. Lin, P.Y. Qian, Five new amicoumacins isolated from a marine-derived bacterium Bacillus subtilis, Mar. Drugs 10 (2) (2012) 319-328.

[69] M. Hashimoto, T. Taguchi, S. Nishida, K. Ueno, K. Koizumi, M. Aburada, K. Ichinose, Isolation of 8-phosphate ester derivatives of amicoumacins: Structure-activity relationship of hydroxy amino acid moiety, J. Antibiot. 60 (12) (2007) 752-756.

[70] K. Krohn, R. Bahramsari, U. Flörke, K. Ludewig, C. Kliche-Spory, A. Michel, H.J. Aust, S. Draeger, B. Schulz, S. Antus, Dihydroisocoumarins fromfungi: isolation, structure elucidation, circular dichroism and biological activity, Phytochemistry 45 (2) (1997) 313-320.

[71] I.V. Pinchuk, P. Bressollier, B. Verneuil, B. Fenet, I.B. Sorokulova, F. Mégraud, M.C. Urdaci, In vitro anti-Helicobacter pylori activity of the probiotic strain Bacillus subtilis 3 is due to secretion of antibiotics, Antimicrob. Agents Chemother. 45 (11) (2001) 3156-3161.

[72] J. Sholi, H. Hinoo, Y. Wakisaka, K. Koizumi, M. Mayama, Isolation of a new peptide antibiotic TL-119, J. Antibiot. 28 (2) (1974) 126-128.

[73] Y. Nakagawa, T. Nakazawa, J. Shoji, On the structure of a new TL-119 antibiotic, J. Antibiot. 28 (12) (1975) 1004-1005.

[74] Y. Kitajima, M.Waki, J. Shoji, T. Ueno, N. Izumiya, Revised structure of the peptide lactone antibiotic, TL-119 and/or A-3302-B, FEBS Lett. 270 (2) (1990) 139-142.

[75] S.K. Bose, S.K. Majumdar, Mycobacillin, a new antifungal antibiotic produced by B. subtilis, Nature 181 (4602) (1958) 134-135.

[76] S.K. Majumda, S.K. Bose, Amino acid sequence in mycobacillin, Biochem. J. 74 (1960) 596-599.

[77] S. Sengupta, A.B. Banerjee, S.K. Bose, Gamma-glutamyl and D- or L-peptide linkages in mycobacillin, a cyclic peptide antibiotic, Biochem. J. 121 (1971) 839-845.

[78] C. Prasad, Bioactive cyclic dipeptides, Peptides 16 (1) (1995) 151-164.

[79] M.B. Martins, L. Carvalho, Diketopiperazines: Biological activity and synthesis, Tetrahedron 63 (40) (2007) 9923-9932.

[80] B. Di Blasio, V. Pavone, F. Nastri, C. Isernia, M. Saviano, C. Pedone, V. Cucinotta, G. Impellizzeri, E. Rizzarelli, G. Vecchio, Conformation for a β-cyclodextrin monosubstituted with a cyclic dipeptide, Proc. Natl. Acad. Sci. 89 (1992) 7218-7221.

[81] K.S. Nishanth, C. Mohandas, J.V. Siji, K.N. Rajasekharan, B. Nambisan, Identification of antimicrobial compound, diketopiperazines, from a Bacillus sp. N strain associated with a rhabditid entomopathogenic nematode against major plant pathogenic fungi, J. Appl. Microbiol. 113 (4) (2012) 914-924.

[82] K.H. Rhee, Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties, Int. J. Antimicrob. Agents 24 (5) (2004) 423-427.

[83] H. Kanzaki, H. Imura, T. Nitoda, K. Kawazu, Enzymatic conversion of cyclic dipeptides to dehydro derivatives that inhibit cell division, J. Biosci. Bioeng. 90 (1) (2000) 86-89.

[84] B. Nicholson, G.K. Lloyd, B.R. Miller, M.A. Palladino, Y. Kiso, Y. Hayashi, S.T. Neuteboom, NPI-2358 is a tubulin-depolymerizing agent: in-vitro evidence for activity as a tumor vascular-disrupting agent, Anticancer Drugs 17 (1) (2006) 25-31.

[85] E. van der Merwe, D. Huang, D. Peterson, G. Kilian, P.J. Milne, M. Van de Venter, C. Frost, The synthesis and anticancer activity of selected diketopiperazines, Peptides 29 (8) (2008) 1305-1311.

[86] F. Fdhila, V. Vázquez, J.L. Sánchez, R. Riguera, DD-Diketopiperazines: Antibiotics active against Vibrio anguillarum isolated from marine bacteria associated with cultures of Pecten maximus, J. Nat. Prod. 66 (10) (2003) 1299-1301.

[87] R.P. Ross, S. Morgan, C. Hill, Preservation and fermentation: Past, present and future, Int. J. Food Microbiol. 79 (2002) 3-16.

[88] J.I. Nagao, Properties and applications of lantibiotics, a class of bacteriocins produced by gram-positive bacteria, J. Oral Biosci. 51 (3) (2009) 158-164.

[89] N. Zimmermann, J.W. Metzger, G. Jung, The tetracyclic lantibiotic actagardine 1HNMR and 13C-NMR assignments and revised primary structure, Eur. J. Biochem. 228 (1995) 786-797.

[90] H.G. Sahl, G. Bierbaum, Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from gram-positive bacteria, Annu. Rev. Microbiol. 52 (1998) 41-79.

[91] A. Guder, T. Schmitter, I. Wiedemann, H.G. Sahl, G. Bierbaum, Role of the single regulatorMrsR1 and the two-component systemMrsR2/K2 in the regulation ofmersacidin production and immunity, Appl. Environ. Microbiol. 68 (1) (2002) 106-113.

[92] R. Bauer, L.M. Dicks, Mode of action of lipid II-targeting lantibiotics, Int. J. Food Microbiol. 101 (2) (2005) 201-216.

[93] C. Klein, K.D. Entian, Genes involved in self-protection against the ATCC 6633, Appl. Environ. Microbiol. 60 (8) (1994) 2793-2801.

[94] S. Chatterjee, D.K. Chatterjee, R.H. Jani, J. Blumbach, B.N. Ganguli, N. Klesel, M. Limbert, G. Seibert, Mersacidin, a new antibiotic from Bacillus. In vitro and in vivo antibacterial activity, J. Antibiot. 45 (6) (1992) 839-845.

[95] S. Chatterjee, S. Chatterjee, S.J. Lad, M.S. Phansalkar, R.H. Rupp, B.N. Ganguli, H.W. Fehlhaber, H. Kogler,Mersacidin, a newantibiotic fromBacillus. Fermentation, isolation, purification and chemical characterization, J. Antibiot. 45 (6) (1992) 832-838.

[96] S.H. Paik, Identification and characterization of the structural and transporter genes for, and the chemical and biological properties of, Sublancin 168, a novel lantibiotic produced by Bacillus subtilis 168, J. Biol. Chem. 273 (36) (1998) 23134-23142.

[97] S.W. Fuchs, T.W. Jaskolla, S. Bochmann, P. Kötter, T.Wichelhaus, M. Karas, T. Stein, K.D. Entian, Entianin, a novel subtilin-like lantibiotic from Bacillus subtilis subsp. spizizenii DSM 15029T with high antimicrobial activity, Appl. Environ. Microbiol. 77 (5) (2011) 1698-1707.

[98] M.M. Theron, J.F.R. Lues, Organic acids and meat preservation: A review, Food Rev. Int. 23 (2) (2007) 141-158.

[99] E. Scallan, R.M. Hoekstra, F.J. Angulo, R.V. Tauxe, M.A. Widdowson, S.L. Roy, J.L. Jones, P.M. Griffin, Foodborne illness acquired in the United States—major pathogens, Emerg. Infect. Dis. 17 (1) (2011) 7-15.

[100] J. Nagao, S.M. Asaduzzaman, Y. Aso, K. Okuda, J. Nakayama, K. Sonomoto, Lantibiotics: Insight and foresight for new paradigm, J. Biosci. Bioeng. 102 (3) (2006) 139-149.

[101] A.A. Andersen, Effect of subtilin on sporees of Clostridium botulinum, J. Bacteriol. 64 (2) (1952) 145-149.

[102] T. Stein, S. Borchert, B. Conrad, J. Feesche, B. Hofemeister, J. Hofemeister, K.D. Entian, Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3, J. Bacteriol. 184 (6) (2002) 1703-1711.

[103] T. Stein, S. Borchert, B. Conrad, J. Feesche, B. Hofemeister, J. Hofemeister, K.D. Entian, Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3, J. Bacteriol. 184 (2002) 1703-1711.

[104] G.B.H. Briitz, K.P.K.H.G. Sahl, Cloning, sequencing and production of the lantibiotic mersacidin, FEMS Lett. 127 (1995) 121-126.

[105] C. Szekat, R.W. Jack, D. Skutlarek, H. Färber, G. Bierbaum, Construction of an expression system for site-directed mutagenesis of the lantibiotic mersacidin, Appl. Environ. Microbiol. 69 (7) (2003) 3777-3783.

[106] W.W. Niu, H.C. Neu, Activity ofmersacidin, a novel peptide, compared with that of vancomycin, teicoplanin, and daptomycin, Antimicrob. Agents Chemother. 35 (5) (1991) 998-1000.

[107] M.S. Barrett, R.P.Wenzel, R.N. Jones, In vitro activity of mersacidin (M87-1551), an investigational peptide antibiotic tested against gram-positive bloodstream isolates, Diagn. Microbiol. Infect. Dis. 15 (7) (1992) 641-644.

[108] D. Kruszewska, H.G. Sahl, G. Bierbaum, U. Pag, S.O. Hynes, A. Ljungh, Mersacidin eradicates methicillin-resistant Staphylococcus aureus (MRSA) in a mouse rhinitis model, J. Antimicrob. Chemother. 54 (3) (2004) 648-653.

[109] H.F. Chambers, The changing epidemiology of Staphylococcus aureus? Emerg. Infect. Dis. 7 (2) (2001) 178-182.

[110] H. Brötz, G. Bierbaum, P.E. Reynolds, H.G. Sahl, The lantibiotic mersacidin inhibits peptidoglycan biosynthesis at the level of transglycosylation, Eur. J. Biochem. 246 (1997) 193-199.

[111] R. Dorenbos, T. Stein, J. Kabel, Thiol-disulfide oxidoreductases are essential for the production of the lantibiotic sublancin 168, J. Biol. Chem. 277 (19) (2002) 16682-16688.

[112] T.J. Oman, J.M. Boettcher, H. Wang, X.N. Okalibe, W.A. van der Donk, Sublancin is not a lantibiotic but an S-linked glycopeptide, Nat. Chem. Biol. 7 (2011) 78-80.

[113] H. Katayama, Y. Asahina, H. Hojo, Chemical synthesis of the S-linked glycopeptide, sublancin, J. Pept. Sci. 17 (12) (2011) 818-821.

[114] H. Wang, W.A. van der Donk, Substrate selectivity of the sublancin Sglycosyltransferase, J. Am. Chem. Soc. 133 (41) (2011) 16394-16397.

[115] Y.S. Hsieh, B.L. Wilkinson, M.R. O'Connell, J.P. Mackay, J.M. Matthews, R.J. Payne, Synthesis of the bacteriocin glycopeptide sublancin 168 and S-glycosylated variants, Org. Lett. 14 (7) (2012) 1910-1913.

[116] G. Zheng, L.Z. Yan, J.C. Vederas, P. Zuber, Genes of the sbo-alb locus of Bacillus subtilis are required for production of the antilisterial bacteriocin subtilosin, J. Bacteriol. 181 (23) (1999) 7346-7355.

[117] J.Y. Dubois, T.R. Kouwen, A.K. Schurich, C.R. Reis, H.T. Ensing, E.N. Trip, J.C. Zweers, J.M. van Dijl, Immunity to the bacteriocin sublancin 168 is determined by the SunI (YolF) protein of Bacillus subtilis, Antimicrob. Agents Chemother. 53 (2) (2009) 651-661.

[118] G. Zheng, R. Hehn, P. Zuber, Mutational analysis of the sbo-alb locus of Bacillus subtilis: Identification of genes required for subtilosin production and immunity, J. Bacteriol. 182 (11) (2000) 3266-3273.

[119] K. Babasaki, T. Takao, Y. Shimonishi, K. Kurahashi, Subtilosin A, a new antibiotic peptide produced by Bacillus subtilis 168: Isolation, structural analysis, and biogenesis, J. Biochem. 98 (3) (1985) 585-603.

[120] R.Marx, T. Stein, K.D. Entian, S.J. Glaser, Structure of the Bacillus subtilis peptide antibiotic subtilosin A determined by 1H-NMR and matrix assisted laser desorption/ ionization time-of-flight mass spectrometry, J. Protein Chem. 20 (4) (2001) 501-506.

[121] K. Kawulka, T. Sprules, R.T. McKay, P. Mercier, C.M. Diaper, P. Zuber, J.C. Vederas, Structure of subtilosin A, an antimicrobial peptide from Bacillus subtilis with unusual posttranslational modifications linking cysteine sulfurs to α-carbons of phenylalanine and threonine, J. Am. Chem. Soc. 125 (2003) 4726-4727.

[122] K.E. Kawulka, T. Sprules, C.M. Diaper, R.M.Whittal, R.T. McKay, P. Mercier, P. Zuber, J.C. Vederas, Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to R-carbon cross-links: Formation and reduction of α-thio-α-amino acid derivatives, Biochemistry 43 (2004) 3385-3395.

[123] S. Thennarasu, D.K. Lee, A. Poon, K.E. Kawulka, J.C. Vederas, A. Ramamoorthy,Membrane permeabilization, orientation, and antimicrobial mechanism of subtilosin A, Chem. Phys. Lipids 137 (1-2) (2005) 38-51.

[124] C.E. Shelburne, F.Y. An, V. Dholpe, A. Ramamoorthy, D.E. Lopatin, M.S. Lantz, The spectrum of antimicrobial activity of the bacteriocin subtilosin A, J. Antimicrob. Chemother. 59 (2) (2007) 297-300.

[125] N. Dahiya, R. Tewari, G.S. Hoondal, Biotechnological aspects of chitinolytic enzymes: a review, Appl. Microbiol. Biotechnol. 71 (6) (2006) 773-782.

[126] P.R. Taylor, S.V. Tsoni, J.A.Willment, K.M. Dennehy, M. Rosas, H. Findon, K. Haynes, C. Steele, M. Botto, S. Gordon, G.D. Brown, Dectin-1 is required for β-glucan recognition and control of fungal infection, Nat. Immunol. 8 (1) (2007) 31-38.

[127] L.M. de la Vega, J.E. Barboza-Corona, M.G. Aguilar-Uscanga, M. Ramírez-Lepe, Purification and characterization of an exochitinase from Bacillus thuringiensis subsp. aizawai and its action against phytopathogenic fungi, Can. J. Microbiol. 52 (7) (2006) 651-657.

[128] D. Liu, J. Cai, C.C. Xie, C. Liu, Y.H. Chen, Purification and partial characterization of a 36-kDa chitinase from Bacillus thuringiensis subsp. colmeri, and its biocontrol potential, Enzyme Microb. Technol. 46 (3-4) (2010) 252-256.

[129] K. Gustafson,M. Roman,W. Fenical, The macrolactins, a novel class of antiviral and cytotoxic macrolides from a deep-sea marine bacterium, J. Am. Chem. Soc. 111 (1989) 7519-7524.

[130] C. Jaruchoktaweechai, K. Suwanborirux, S. Tanasupawatt, P. Kittakoop, P. Menasveta, New macrolactin from a marine Bacillus sp. Sc026, J. Nat. Prod. 63 (2000) 964-966.

[131] M.R. Romero-Tabarez, R. Jansen, M. Sylla, H. Lünsdorf, S. Häussler, D.A. Santosa, K.N. Timmis, G.Molinari, 7-O-malonylmacrolactin A, a new macrolactin antibiotic from Bacillus subtilis active against methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and a small-colony variant of Burkholderia cepacia, Antimicrob. Agents Chemother. 50 (5) (2006) 1701-1709.

[132] T. Nagao, K. Adachi, M. Sakai, M. Nishijima, H. Sano, Novel macrolactins as antibiotic lactones from a marine bacterium, J. Antibiot. 54 (4) (2001) 333-339.

[133] M.A. Mondol, F.S. Tareq, J.H. Kim, Ma Lee, H.S. Lee, Y.J. Lee, J.S. Lee, H.J. Shin, Cyclic ether-containingmacrolactins, antimicrobial 24-membered isomericmacrolactones from a marine Bacillus sp. J. Nat. Prod. 74 (12) (2011) 2582-2587.

[134] M.A. Mondol, J.H. Kim, H.S. Lee, Y.J. Lee, H.J. Shin, Macrolactin W, a new antibacterial macrolide from a marine Bacillus sp. Bioorg. Med. Chem. Lett. 21 (12) (2011) 3832-3835.

[135] M. Georgy, P. Lesot, J.M. Campagne, Synthetic studies on macrolactin A construction of C4-C24 fragment, J. Org. Chem. 72 (2007) 3543-3549.

[136] K. Schneider, X.H. Chen, J. Vater, P. Franke, G. Nicholson, R. Borriss, R.D. Süssmuth, Macrolactin is the polyketide biosynthesis product of the pks2 cluster of Bacillus amyloliquefaciens FZB42, J. Nat. Prod. 70 (2007) 1417-1423.

[137] B.S. Zimmerman, C.D. Schwartz, R.L. Monaghan, Difficidin and oxydifficidin: A novel broad spectrum antibacterial antibiotics produced by Bacillus subtilis, J. Antibiot. 40 (12) (1986) 1677-1681.

[138] X.H. Chen, R. Scholz,M. Borriss, H. Junge, G.Mögel, S. Kunz, R. Borriss, Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease, J. Biotechnol. 140 (1-2) (2009) 38-44.

[139] A. Hamdache, A. Lamarti, J. Aleu, I.G. Collado, Non-peptide metabolites from the genus Bacillus, J. Nat. Prod. 74 (4) (2011) 893-899.

[140] P.S. Patel, S. Huang, S. Fisher, D. Pirnik, C. Aklonis, L. Dean, E. Meyers, P. Fernandes, F. Mayerl, Bacillaene, a novel inhibitor of procaryotic protein synthesis produced by Bacillus subtilis: Production, taxonomy, isolation, physico-chemical characterization and biological activity, J. Antibiot. 48 (9) (1995) 997-1003.

[141] R.A. Butcher, F.C. Schroeder, M.A. Fischbach, P.D. Straight, R. Kolter, C.T. Walsh, J. Clardy, The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis, Proc. Natl. Acad. Sci. 104 (5) (2007) 1506-1509.

[142] N. Tamehiro, Y. Okamoto-Hosoya, S. Okamoto, M. Ubukata, M. Hamada, H. Naganawa, K. Ochi, Bacilysocin, a novel phospholipid antibiotic produced by Bacillus subtilis 168, Antimicrob. Agents Chemother. 46 (2) (2002) 315-320.

[143] T. Inaoka, K. Ochi, Glucose uptake pathway-specific regulation of synthesis of neotrehalosadiamine, a novel autoinducer produced in Bacillus subtilis, J. Bacteriol. 189 (1) (2007) 65-75.

[144] T. Tsuno, C. Ikeda, K. Numata, K. Tomita, K. Konishi, K. Kawaguchi, 3,3′-Neotrehal osadiamine (BMY-28251)+, a new aminosugar antibiotic, J. Antibiot. 39 (7) (1996) 1001-1003.

[145] T. Inaoka, K. Takahashi, H. Yada, M. Yoshida, K. Ochi, RNA polymerase mutation activates the production of a dormant antibiotic 3,3′-neotrehalosadiamine via an autoinduction mechanism in Bacillus subtilis, J. Biol. Chem. 279 (5) (2004) 3885-3892.

[146] L.Z. Li, H. Zheng, Y.J. Yuan, Effects of propionate on streptolydigin production and carbon flux distribution in streptomyces zydicus AS 4.2501, Chin. J. Chem. Eng. 15 (2) (2007) 143-149.

[147] D.G. Cooper, C.R. Macdonald, S.J. Duff, N. Kosaric, Enhanced production of surfactin from Bacillus subtilis by continuous product removal and metal cation additions, Appl. Environ. Microbiol. 42 (3) (1981) 408-412.

[148] I. Noriyasu, S.R. Mohammad, A. Takashi, Production of iturin A homologues under different culture conditions, J. Environ. Sci. (China) 21 (2009) 28-32.

[149] Q.L. Ren, H.B. Xing, Z.b Bao, B.G. Su, Q.W. Yang, Y.W. Yang, Z.G. Zhang, Recent advances in separation of bioactive natural products, Chin. J. Chem. Eng. 21 (9) (2013) 937-952.

[150] I. Grangemard, F. Peypoux, J. Wallach, B.C. Das, H. Labbé, A. Caille, M. Genest, R. Maget-Dana, M. Ptak, J.M. Bonmatin, Lipopeptides with improved properties: Structure by NMR, purification by HPLC and structure-activity relationships of new isoleucyl-rich surfactins, J. Pept. Sci. 3 (1997) 145-154.

[151] A. Hamdache, R. Azarken, A. Lamarti, J. Aleu, I.G. Collado, Comparative genome analysis of Bacillus spp. and its relationship with bioactive nonribosomal peptide production, Phytochem. Rev. (2013). http://dx.doi.org/10.1007/s11101-013-9278-4.

[152] S.A. Mahlstedt, C.T. Walsh, Investigation of anticapsin biosynthesis reveals a fourenzyme pathway to tetrahydrotyrosine in Bacillus subtilis, Biochemistry 49 (5) (2010) 912-923.

[153] J.B. Parker, C.T. Walsh, Stereochemical outcome at four stereogenic centers during conversion of prephenate to tetrahydrotyrosine by BacABGF in the bacilysin pathway, Biochemistry 51 (2012) 5622-5632.

[154] M. Rajavel, K. Perinbam, B. Gopal, Structural insights into the role of Bacillus subtilis YwfH (BacG) in tetrahydrotyrosine synthesis, Acta Crystallogr. D 69 (2013) 324-332.

[155] T. Inaoka, T. Satomura, Y. Fujita, K. Ochi, Novel gene regulation mediated by overproduction of secondary metabolite neotrehalosadiamine in Bacillus subtilis, FEMS Microbiol. Lett. 291 (2) (2009) 151-156.

[156] S. Heinzmann, K.D. Entian, T. Stein, Engineering Bacillus subtilis ATCC 6633 for improved production of the lantibiotic subtilin, Appl. Microbiol. Biotechnol. 69 (5) (2006) 532-536.

[157] L. Roland, Overcoming antimicrobial resistance: Profile of a new ketolide antibacterial, telithromycin, J. Antimicrob. Chemother. 48 (2001) 9-23.

[158] D. Felmingham, G. Zhanel, D. Hoban, Activity of the ketolide antibacterial telithromycin against typical community-acquired respiratory pathogens, J. Antimicrob. Chemother. 48 (2001) 33-42.

[159] A. Bonnefoy, M. Guitton, C. Delachaume, L.P. Priol, A.M. Girard, In vivo efficacy of the new ketolide telithromycin (HMR 3647) in murine infection models, Antimicrob. Agents Chemother. 45 (6) (2001) 1688-1692.

[160] W.J. Geldenhuys, A. Bishayee, A.S. Darvesh, R.T. Carroll, Natural products of dietary origin as lead compounds in virtual screening and drug design, Curr. Pharm. Biotechnol. 13 (1) (2012) 117-124.

[161] C.W. Murray, D.C. Rees, The rise of fragment-based drug discovery, Nat. Chem. 1 (2009) 187-192.

[162] C.W. Murray, T.L. Blundell, Structural biology in fragment-based drug design, Curr. Opin. Struct. Biol. 20 (2010) 497-507.

[163] Z. Han, J.S. Pinkner, B. Ford, R. Obermann, W. Nolan, S.A. Wildman, D. Hobbs, T. Ellenberger, C.K. Cusumano, S.J. Hultgren, J.W. Janetka, Structure-based drug design and optimization of mannoside bacterial FimH antagonists, J. Med. Chem. 53 (12) (2010) 4779-4792.

Natural products from Bacillus subtilis with antimicrobial properties

Natural products from Bacillus subtilis with antimicrobial properties

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