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Secondary metabolites of soil Bacillus spp.

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Abstract

Bacillus species produce secondary metabolites that are the object of natural product chemistry studies. The wide structural variability of these compounds has attracted the curiosity of chemists and their biological activities have inspired the pharmaceutical industry to search for lead structures in microbial extracts. Screening of microbial extracts reveals the large structural diversity of natural compounds with broad biological activities, such as antimicrobial, antiviral, immunosuppressive, and antitumor activities, that enable the bacterium to survive in its natural environment. These findings widen the potential industrial importance of Bacillus spp., particularly of B. thuringiensis, beyond insecticidal usage and may help explain the role of Bacillus spp. in the soil ecosystem.

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References

  • Ahern M, Verschueren S, van Sinderen D (2003) Isolation and characterisation of a novel bacteriocin produced by Bacillus thuringiensis strain B439. FEMS Microbiol Lett 220:127–131

    Article  PubMed  CAS  Google Scholar 

  • Aranda FJ, Teruel JA, Ortiz A (2005) Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochim Biophys Acta 1713:51–56

    Article  PubMed  CAS  Google Scholar 

  • Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Fact 8:63–74

    Article  PubMed  Google Scholar 

  • Awais M, Pervez A, Qayyum S, Saleem M (2008) Effects of glucose, incubation period and pH on the production of peptide antibiotics by Bacillus pumilus. African J Microbiol Res 2:114–119

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bizani D, Dominguez APM, Brandelli A (2005a) Purification and partial chemical characterization of the antimicrobial peptide cerein 8A. Lett Appl Microbiol 41:269–273

    Article  PubMed  CAS  Google Scholar 

  • Bizani D, Motta AS, Morrissy JAC, Terra RMS, Souto AA, Brandelli A (2005b) Antibacterial activity of cerein 8A, a bacteriocin-like peptide produced by Bacillus cereus. Int Microbiol 8:125–131

    PubMed  CAS  Google Scholar 

  • Bode HB (2009) Entomopathogenic bacteria as a source of secondary metabolites. Curr Opin Chem Biol 13:224–230

    Article  PubMed  CAS  Google Scholar 

  • Calugay RJ, Takeyama H, Mukoyama D, Fukuda Y, Suzuki T, Kanoh K, Matsunaga T (2006) Catechol siderophore excretion by magnetotactic bacterium Magnetospirillum magneticum AMB-1. J Biosci Bioeng 101:445–447

    Article  PubMed  CAS  Google Scholar 

  • Carrillo C, Teruel JA, Aranda FJ, Ortiz A (2003) Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim Biophys Acta 1611:91–97

    Article  PubMed  CAS  Google Scholar 

  • Che Y, Deng Y, Wang J, Cai J, Ren G (2004) Characterization of melanin produced by a wild-type strain of bacillus thuringiensis. J Gen Appl Microbiol 50:183–188

    Article  Google Scholar 

  • Chehimi S, Delalande F, Sablé S, Hajlaoui M-R, Van Dorsselaer A, Limam F, Pons A-M (2007) Purification and partial amino acid sequence of thuricin S, a new anti-Listeria bacteriocin from Bacillus thuringiensis. Can J Microbiol 53:284–290

    Article  PubMed  CAS  Google Scholar 

  • Chen G, Wang G-Y-S, Li X, Waters B, Davies J (2000) Enhanced production of microbial metabolites in the presence of dimethyl sulfoxide. J Antibiot 53:1145–1153

    PubMed  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Süssmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014

    Article  PubMed  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Borriss R (2009) More than anticipated_production of antibiotics and other secondary metabolites by Bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol 16:14–24

    Article  PubMed  CAS  Google Scholar 

  • Cherif A, Ouzari H, Daffonchio D, Cherif H, Slama KB, Hassen A, Jaoua S, Boudabous A (2001) Thuricin 7: a novel bacteriocin produced by Bacillus thuringiensis BMG1.7, a new strain isolated from soil. Lett Appl Microbiol 32:243–247

    Article  PubMed  CAS  Google Scholar 

  • Cherif A, Chehimi S, Limem F, Hansen BM, Hendriksen NB, Daffonchio D, Boudabous A (2003) Detection and characterization of the novel bacteriocin entomocin 9, and safety evaluation of its producer, Bacillus thuringiensis ssp. entomocidus HD9. J Appl Microbiol 95:990–1000

    Article  PubMed  CAS  Google Scholar 

  • Chmara H, Milewski S, Dzieduszycka M, Smulkowski M, Sawlewicz P, Borowski E (1982) Epoxypeptides—a novel group of metabolic inhibitors in procaryotic and eucaryotic organisms. Drugs Exp Clin Res 8:11–12

    CAS  Google Scholar 

  • Claus D, Berkeley RCW (1986) Genus Bacillus Cohn 1872. In: Sneath PHA et al (eds) Bergey’s Manual of Systematic Bacteriology. William and Wilkins, Baltimore, pp 1105–1139

    Google Scholar 

  • Das P, Mukherjee S, Sen R (2008) Genetic regulations of the biosynthesis of microbial surfactants: an overview. Biotechnol Genet Eng Rev 25:165–186

    Article  PubMed  CAS  Google Scholar 

  • Demain AL, Fang A (2000) The natural functions of secondary metabolites. In: Scheper T (ed) Advances in biochemical engineering/biotechnology, vol 69. Springer, Berlin, pp 1–39

    Google Scholar 

  • Espinasse S, Gohar M, Lereclus D, Sanchis V (2002) An ABC transporter from Bacillus thuringiensis is essential for B-exotoxin I production. J Bacteriol 184:5848–5854

    Article  PubMed  CAS  Google Scholar 

  • Espinasse S, Gohar M, Lereclus D, Sanchis V (2004) An extracytoplasmic-function sigma factor is involved in a pathway controlling β-Exotoxin I production in Bacillus thuringiensis subsp. thuringiensis Strain 407–1. J Bacteriol 186:3108–3116

    Article  PubMed  CAS  Google Scholar 

  • Favret ME, Yousten AA (1989) Thuricin: the bacteriocin produced by Bacillus thuringiensis. J Invert Pathol 53:206–216

    Article  CAS  Google Scholar 

  • Grangemard I, Wallach J, Maget-Dana R, Peypoux F (2001) Lichenysin: a more efficient cation chelator than surfactin. Appl Biochem Biotechnol 90:199–210

    Article  PubMed  CAS  Google Scholar 

  • Gross H (2007) Strategies to unravel the function of orphan biosynthesis pathways: recent examples and future prospects. Appl Microbiol Biotechnol 75:267–277

    Article  PubMed  CAS  Google Scholar 

  • Han JS, Cheng JH, Yoon TM, Song J, Rajkarnikar A, Kim WG, Yoo ID, Yang YY, Suh JW (2005) Biological control agent of common scab disease by antagonistic strain Bacillus sp. sunhua. J Appl Microbiol 99:213–221

    Article  PubMed  CAS  Google Scholar 

  • Hathout Y, Ho Y-P, Ryzhov V, Demirev P, Fenselau C (2000) Kurstakin: a new class of lipopeptides isolated from Bacillus thuringiensis. J Nat Prod 63:1492–1496

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Inaoka T, Takahashi K, Ohnishi-Kameyama M, Yoshida M, Ochi K (2003) Guanine nucleotides guanosine 5′-diphosphate 3′-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. J Biol Chem 278:2169–2176

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jacques P, Hbid C, Destain J, Razafindralambo H, Paquot M, De Pauw E, Thonart P (1999) Optimization of biosurfactant lipopeptide production from Bacillus subtilis S499 by Plackett-Burman design. Appl Biochem Biotechnol 77–79:223–233

    Article  Google Scholar 

  • Jaruchoktaweechai CS, Suwanboriux K, Tanasupawatt S, Kittakoop P, Menasveta P (2000) New macrolactins from a marine Bacillus sp. Sc026. J Nat Prod 63:984–986

    Article  PubMed  CAS  Google Scholar 

  • Kalinovskaya N, Kuznetsova TA, Ivanova EP, Romanenko LA, Voinov VG, Huth F, Laatsch H (2002) Characterization of surfactin-like cyclic depsipeptides synthesized by Bacillus pumilus Ascidian Halocynthia aurantium. Mar Biotechnol (NY) 4:179–189

    Article  CAS  Google Scholar 

  • Kamoun F, Mejdoub H, Aouissaoui H, Reinbolt J, Hammami A, Jaoua S (2005) Purification, amino acid sequence and characterization of bacthuricin F4, a new bacteriocin produced by Bacillus thuringiensis. J Appl Microbiol 98:881–888

    Article  PubMed  CAS  Google Scholar 

  • Karlovsky P (2008) Secondary metabolites in soil ecology. In: Karlowsky P (ed) Soil biology, vol 14. Springer-Verlag, Berlin Heidelberg, pp 1–19

    Google Scholar 

  • Kevany BM, Rasko DA, Thomas MG (2009) Characterization of the complete zwittermicin A biosynthesis gene cluster from Bacillus cereus. Appl Environ Microbiol 75:1144–1155

    Article  PubMed  CAS  Google Scholar 

  • Khalil R, Djadouni F, Elbahloul Y, Omar S (2009) The influence of cultural and physical conditions on the antimicrobial activity of bacteriocin produced by a newly isolated Bacillus megaterium 22 strain. African J Food Sci 3:11–22

    CAS  Google Scholar 

  • Kilian M, Steiner U, Krebs B, Junge H, Schmiedeknecht G, Hain R (2000) FZB24® Bacillus subtilis-mode of action of a microbial agent enhancing plant vitality. Pflanzenschutz-Nachrichten 1:72–93

    Google Scholar 

  • Koppisch AT, Dhungana S, Hill KK, Boukhalfa H, Heine HS, Colip LA, Romero RB, Shou Y, Ticknor LO, Marrone BL, Hersman SI, Ruggiero CE (2008a) Petrobactin is produced by both pathogenic and non-pathogenic isolates of the Bacillus cereus group of bacteria. Biometals 21:581–589

    Article  PubMed  CAS  Google Scholar 

  • Koppisch AT, Hotta K, Fox DT, Ruggiero CE, Kim C-Y, Sanchez T, Iyer S, Browder CC, Unkefer PJ, Unkefer CJ (2008b) Biosynthesis of the 3, 4-Dihydroxybenzoate Moieties of Petrobactin by Bacillus anthracis. J Org Chem 73:5759–5765

    Article  PubMed  CAS  Google Scholar 

  • Koumoutsi A, Chen X-H, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borriss R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186:1084–1096

    Article  PubMed  CAS  Google Scholar 

  • Le Marrec C, Hyronimus B, Bressollier P, Verneuil B, Urdaci MC (2000) Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I4. Appl Environ Microbiol 66:5213–5220

    Article  PubMed  CAS  Google Scholar 

  • Lee KH, Jun KD, Kim WS, Paik HD (2001) Partial characterization of polyfermenticin SCD, a newly identified bacteriocin of Bacillus polyfermenticus. Lett Appl Microbiol 32:146–151

    Article  PubMed  CAS  Google Scholar 

  • Lisboa MP, Bonatto D, Bizani D, Henriques JAP, Brandelli A (2006) Characterization of a bacteriocin-like substance produced by Bacillus amyloliquefaciens isolated from the Brazilian Atlantic forest. Int Microbiol 9:111–118

    PubMed  CAS  Google Scholar 

  • Maget-Dana R, Peypoux F (1994) Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87:151–174

    Article  PubMed  CAS  Google Scholar 

  • Moyne AL, Cleveland TE, Tuzun S (2004) Molecular characterization and analysis of the operon encoding the antifungal lipopeptide bacillomycin D. FEMS Microbiol Lett 234:43–49

    Article  PubMed  CAS  Google Scholar 

  • Muthusamy K, Gopalakrishnan S, Ravi TK, Sivachidambaram P (2008) Biosurfactants: properties, commercial production and application. Curr Sci 94:736–747

    CAS  Google Scholar 

  • 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 43:267–280

    PubMed  CAS  Google Scholar 

  • Paik HD, Bae SS, Park SH, Pan JG (1997) Identification and partial characterization of tochicin, a bacteriocin produced by Bacillus thuringiensis subsp. tochigiensis. J Ind Microbiol Biotechnol 19:294–298

    Article  PubMed  CAS  Google Scholar 

  • Pattnaik P, Kaushik JK, Grover S, Batish VK (2001) Purification and characterization of a bacteriocin-like compound (lichenin) produced anaerobically by Bacillus licheniformis isolated from water buffalo. J Appl Microbiol 91:636–645

    Article  PubMed  CAS  Google Scholar 

  • Pinchuk IV, Bressollier P, Sorokulova IB, Verneuil B, Urdaci MC (2002) Amicoumacin antibiotic production and genetic diversity of Bacillus subtilis strains isolated from different habitats. Res Microbiol 153:269–276

    Article  PubMed  CAS  Google Scholar 

  • Pyoung K II, Ryu J, Kim YH, ChI Y-T (2010) Production of biosurfactant lipopeptides Iturin A, Fengycin, and Surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 20:138–145

    Google Scholar 

  • Ramarathnam R, Bo S, Chem Y, Fernando WGD, Xuewen G, de Kievit T (2007) Molecular and biochemical detection of fengycin and bacillomycin D producing bacillus spp., antagonistic to fungal pathogens of canola and wheat. Can J Microbiol 53:901–911

    Article  PubMed  CAS  Google Scholar 

  • Rea MC, Sit CS, Claytona E, O’Connor PM, Whittal RM, Zheng J, Vederas JC, Ross RP, Hill C (2010) Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. PNAS 107:9352–9357

    Article  PubMed  CAS  Google Scholar 

  • Rogers EW, Molinski TF (2007) Asymmetric synthesis of diastereomeric diaminoheptanetetraols. A proposal for the configuration of (+)−Zwittermicin A. Org Lett 9:437–440

    Article  PubMed  CAS  Google Scholar 

  • Rogers EW, Molinski TF (2009) (+)-Zwittermicin A. Rapid assembly of C9–C15 and a formal total synthesis. J Org Chem 74:7660–7664

    Article  PubMed  CAS  Google Scholar 

  • Romero-Tabarez M, Jansen R, Sylla M, Lünsdorf H, Häussler S, Santosa DA, Timmis KN, Molinari G (2006) 7-O-Malonyl macrolactin 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 50:1701–1709

    Article  PubMed  CAS  Google Scholar 

  • Sansinenea E, Vazquez C, Ortiz A (2010) Genetic manipulation in Bacillus thuringiensis for strain improvement. Biotechnol Lett 32:1549–1557

    Article  PubMed  CAS  Google Scholar 

  • Saxena D, Ben-Dov E, Manasherob R, Barak Z, Boussiba S, Zaritsky A (2002) A UV tolerant mutant of Bacillus Thuringiensis subsp. kurstaki producing melanin. Curr Microbiol 44:25–30

    Article  PubMed  CAS  Google Scholar 

  • Shaligram NS, Singhal RS (2010) Surfactin–a review on biosynthesis, fermentation, purification and applications. Food Technol Biotechnol 48:119–134

    CAS  Google Scholar 

  • Silo-Suh LA, Stabb EV, Raffel SJ, Handelsman J (1998) Target range of zwittermicin A, an aminopolyol antibiotic from Bacillus cereus. Curr Microbiol 37:6–11

    Article  PubMed  CAS  Google Scholar 

  • Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857

    Article  PubMed  CAS  Google Scholar 

  • Stein T, Borchert S, Kiesau P, Heinzmann S, Klöss S, Klein C et al (2002) Dual control of subtilin biosynthesis and immunity in Bacillus subtilis. Mol Microbiol 44:403–416

    Article  PubMed  CAS  Google Scholar 

  • Steinborn G, Hajirezaei MR, Hofemeister J (2005) Bac genes for recombinant bacilysin and anticapsin production in Bacillus host strains. Arch Microbiol 183:71–79

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tendulkar SR, Saikuman YK, Patel V, Raghotama S, Munshi TK, Balaram P, Chattoo BB (2007) Isolation, purification and characterization of an antifungal molecule produced by Bacillus licheniformis BC98, and its effect on phytopathogen Magnaporthe grisea. J Appl Microbiol 103:2331–2339

    Article  PubMed  CAS  Google Scholar 

  • Torkar KG, Matijašić BB (2003) Partial characterization of bacteriocins produced by Bacillus cereus isolates from milk and milk products. Food Technol Biotechnol 41:121–129

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tsuno T, Ikeda C, Numata K, Tomita K, Konishi M, Kawaguchi H (1986) 3, 3′-Neotrehalosadiamine (BMY-28251), a new aminosugar antibiotic. J Antibiot 39:1001–1003

    PubMed  CAS  Google Scholar 

  • Velusamy P, Gnanamanickam SS (2008) The Effect of Bacterial Secondary Metabolites on Bacterial and Fungal Pathogens of Rice. In: Karlowsky P (ed) Soil biology, vol 14. Springer-Verlag, Berlin Heidelberg, pp 93–106

    Google Scholar 

  • Woo-Jin J, Mabood F, Souleimanov A, Zhou X, Jaoua S, Kamoun F, Smith DL (2008) Stability and antibacterial activity of bacteriocins produced by Bacillus thuringiensis and Bacillus thuringiensis ssp. Kurstaki. J Microbiol Biotechnol 18:1836–1840

    Google Scholar 

  • Wulff EG, Mguni CM, Mansfeld-Giese K, Fels J, Lübeck M, Hockenhull J (2002) Biochemical and molecular characterization of Bacillus amyloliquefaciens, B. subtilis and B. pumilus isolates with distinct antagonistic potential against Xanthomonas campestris pv. campestris. Plant Patholo 51:574–584

    Article  CAS  Google Scholar 

  • Yang Y-L, Xu Y, Straight P, Dorrestein PC (2009) Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 5:885–887

    Article  PubMed  CAS  Google Scholar 

  • Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL (2002) Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34:955–963

    Article  CAS  Google Scholar 

  • Zawadzka AM, Abergel RJ, Nichiporuk R, Andersen UN, Raymond KN (2009) Siderophore-mediated iron acquisition system in Bacillus cereus: identification of receptors for anthrax virulence-associated petrobactin. Biochemistry 48:3645–3657

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Choi Y-L, Sun M, Yu Z (2008) Novel roles of Bacillus thuringiensis to control plant diseases. Appl Microbiol Biotechnol 80:563–572

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank VIEP (project) and CONACyT (project No 80915) for financial support. We thank to the referees who revised the manuscript and made a great effort to improve it. We want to give a special acknowledgement to Dr. Ernest Schnepf for proofreading the manuscript improving it.

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  1. Facultad de Ciencias Químicas de la Benemérita Universidad Autónoma de Puebla, 72570, Puebla, PUE, México

    Estibaliz Sansinenea & Aurelio Ortiz

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  1. Estibaliz Sansinenea
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  2. Aurelio Ortiz
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Correspondence to Estibaliz Sansinenea.

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Sansinenea, E., Ortiz, A. Secondary metabolites of soil Bacillus spp.. Biotechnol Lett 33, 1523–1538 (2011). https://doi.org/10.1007/s10529-011-0617-5

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