Abstract
Overuse of broad-spectrum antibiotics to control human and plant pathogens greatly accelerated the development of antibiotic resistance among bacteria and fungi. Therefore, usage of new approaches is necessary to control outbreaks of phytopathogenic diseases as well as multidrug-resistant human pathogens. Many of the polyketides (PKs) and lipopetides (LPs) produced by Bacillus and Paenibacillus species have been described as antimicrobial agents that can be potentially applied as sustainable bio-organic products in medicine against human pathogens and in agriculture for controlling plant pathogens. The present review provides a general information about the classification and biochemical structure of known Bacillus- and Paenibacillus-secreted PKs, as well as ribosomally and nonribosomally synthesized peptides, their functional features, gene clusters involved in their production, and the mode of action of these metabolites.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abriouel H, Franz CM, Ben Omar N, Galvez A (2011) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35(1):201–232. https://doi.org/10.1111/j.1574-6976.2010.00244.x
Acedo JZ, Chiorean S, Vederas JC, van Belkum MJ (2018) The expanding structural variety among bacteriocins from Gram-positive bacteria. FEMS Microbiol Rev 42(6):805–828. https://doi.org/10.1093/femsre/fuy033
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(1):127–131
Aleti G, Sessitsch A, Brader G (2015) Genome mining: prediction of lipopeptides and polyketides from Bacillus and related Firmicutes. Comput Struct Biotechnol J 13:192–203. https://doi.org/10.1016/j.csbj.2015.03.003
Alkhalili RN, Canback B (2018) Identification of putative novel class-I Lanthipeptides in firmicutes: a combinatorial in silico analysis approach performed on genome sequenced bacteria and a close inspection of Z-geobacillin lanthipeptide biosynthesis gene cluster of the thermophilic Geobacillus sp. strain ZGt-1. Int J Mol Sci 19(9). https://doi.org/10.3390/ijms19092650
Arguelles Arias A, Ongena M, Devreese B, Terrak M, Joris B, Fickers P (2013) Characterization of amylolysin, a novel lantibiotic from Bacillus amyloliquefaciens GA1. PLoS One 8(12):e83037. https://doi.org/10.1371/journal.pone.0083037
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 Factories 8:63. https://doi.org/10.1186/1475-2859-8-63
Arias AA, Joris B, Fickers P (2014) Dual mode of action of amylolysin: a type-B lantibiotic produced by Bacillus amyloliquefaciens GA1. Protein Pept Lett 21(4):336–340. https://doi.org/10.2174/09298665113206660102
Ash C, Farrow J, Wallbanks S, Collins M (1991) Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit-ribosomal RNA sequences. Lett Appl Microbiol 13(4):202–206
Ash C, Priest FG, Collins MD (1993) Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Antonie Van Leeuwenhoek 64(3):253–260. https://doi.org/10.1007/bf00873085
Awais M, Shah AA, Hameed A, Hasan F (2007) Isolation, identification and optimization of bacitracin produced by Bacillus sp. Pak J Bot 39(4):1303
Babasaki K, Takao T, Shimonishi Y, Kurahashi K (1985) Subtilosin A, a new antibiotic peptide produced by Bacillus subtilis 168: isolation, structural analysis, and biogenesis. J Biochem 98(3):585–603
Baindara P, Chaudhry V, Mittal G, Liao LM, Matos CO, Khatri N, Franco OL, Patil PB, Korpole S (2016) Characterization of the antimicrobial peptide penisin, a class Ia novel lantibiotic from Paenibacillus sp. strain A3. Antimicrob Agents Chemother 60(1):580–591. https://doi.org/10.1128/aac.01813-15
Barbosa J, Caetano T, Mendo S (2015) Class I and class II lanthipeptides produced by Bacillus spp. J Nat Prod 78(11):2850–2866. https://doi.org/10.1021/np500424y
Beatty PH, Jensen SE (2002) Paenibacillus polymyxa produces fusaricidin-type antifungal antibiotics active against Leptosphaeria maculans, the causative agent of blackleg disease of canola. Can J Microbiol 48(2):159–169
Bechet M, Caradec T, Hussein W, Abderrahmani A, Chollet M, Leclere V, Dubois T, Lereclus D, Pupin M, Jacques P (2012) Structure, biosynthesis, and properties of kurstakins, nonribosomal lipopeptides from Bacillus spp. Appl Microbiol Biotechnol 95(3):593–600. https://doi.org/10.1007/s00253-012-4181-2
Begley M, Cotter PD, Hill C, Ross RP (2009) Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl Environ Microbiol 75(17):5451–5460. https://doi.org/10.1128/aem.00730-09
Beric T, Kojic M, Stankovic S, Topisirovic L, Degrassi G, Myers M, Venturi V, Fira D (2012) Antimicrobial activity of Bacillus sp natural isolates and their potential use in the biocontrol of phytopathogenic bacteria. Food Technol Biotechnol 50(1):25–31
Besson F, Peypoux F, Michel G (1978) Action of mycosubtilin and of bacillomycin L on Micrococcus luteus cells and protoplasts: influence of the polarity of the antibiotics upon their action on the bacterial cytoplasmic membrane. FEBS Lett 90(1):36–40
Brotz H, Bierbaum G, Leopold K, Reynolds PE, Sahl HG (1998) The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob Agents Chemother 42(1):154–160
Butcher RA, Schroeder FC, Fischbach MA, Straight PD, Kolter R, Walsh CT, Clardy J (2007) The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc Natl Acad Sci U S A 104(5):1506–1509. https://doi.org/10.1073/pnas.0610503104
Cawoy H, Bettiol W, Fickers P, Ongena M (2011) Bacillus-based biological control of plant diseases. Pesticides in the modern world—pesticides use and management. InTech, Rijeka, pp 273–302
Chehimi S, Delalande F, Sable S, Hajlaoui MR, Van Dorsselaer A, Limam F, Pons AM (2007) Purification and partial amino acid sequence of thuricin S, a new anti-Listeria bacteriocin from Bacillus thuringiensis. Can J Microbiol 53(2):284–290. https://doi.org/10.1139/w06-116
Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Sussmuth RD, Borriss R (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol 188(11):4024–4036. https://doi.org/10.1128/jb.00052-06
Chen H, Wang L, Su CX, Gong GH, Wang P, Yu ZL (2008) Isolation and characterization of lipopeptide antibiotics produced by Bacillus subtilis. Lett Appl Microbiol 47(3):180–186. https://doi.org/10.1111/j.1472-765X.2008.02412.x
Chen XH, Scholz R, Borriss M, Junge H, Mogel G, Kunz S, Borriss R (2009) Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140(1–2):38–44. https://doi.org/10.1016/j.jbiotec.2008.10.015
Chmara H (1985) Inhibition of glucosamine synthase by bacilysin and anticapsin. J Gen Microbiol 131(2):265–271. https://doi.org/10.1099/00221287-131-2-265
Choi SK, Park SY, Kim R, Kim SB, Lee CH, Kim JF, Park SH (2009) Identification of a polymyxin synthetase gene cluster of Paenibacillus polymyxa and heterologous expression of the gene in Bacillus subtilis. J Bacteriol 191(10):3350–3358. https://doi.org/10.1128/jb.01728-08
Cochrane SA, Vederas JC (2016) Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med Res Rev 36(1):4–31. https://doi.org/10.1002/med.21321
Cochrane SA, Lohans CT, van Belkum MJ, Bels MA, Vederas JC (2015a) Studies on tridecaptin B(1), a lipopeptide with activity against multidrug resistant Gram-negative bacteria. Org Biomol Chem 13(21):6073–6081. https://doi.org/10.1039/c5ob00780a
Cochrane SA, Surgenor RR, Khey KM, Vederas JC (2015b) Total synthesis and stereochemical assignment of the antimicrobial lipopeptide cerexin A1. Org Lett 17(21):5428–5431. https://doi.org/10.1021/acs.orglett.5b02779
Cochrane SA, Findlay B, Bakhtiary A, Acedo JZ, Rodriguez-Lopez EM, Mercier P, Vederas JC (2016) Antimicrobial lipopeptide tridecaptin A1 selectively binds to Gram-negative lipid II. Proc Natl Acad Sci U S A 113(41):11561–11566. https://doi.org/10.1073/pnas.1608623113
Cotter PD, Ross RP, Hill C (2013) Bacteriocins—a viable alternative to antibiotics? Nat Rev Microbiol 11(2):95–105. https://doi.org/10.1038/nrmicro2937
Deleu M, Paquot M, Nylander T (2008) Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophys J 94(7):2667–2679. https://doi.org/10.1529/biophysj.107.114090
Ding R, Wu XC, Qian CD, Teng Y, Li O, Zhan ZJ, Zhao YH (2011) Isolation and identification of lipopeptide antibiotics from Paenibacillus elgii B69 with inhibitory activity against methicillin-resistant Staphylococcus aureus. J Microbiol 49(6):942–949. https://doi.org/10.1007/s12275-011-1153-7
Dischinger J, Josten M, Szekat C, Sahl HG, Bierbaum G (2009) Production of the novel two-peptide lantibiotic lichenicidin by Bacillus licheniformis DSM 13. PLoS One 4(8):e6788. https://doi.org/10.1371/journal.pone.0006788
Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359. https://doi.org/10.1146/annurev.phyto.43.032904.092924
Garcia-Gonzalez E, Muller S, Ensle P, Sussmuth RD, Genersch E (2014a) Elucidation of sevadicin, a novel non-ribosomal peptide secondary metabolite produced by the honey bee pathogenic bacterium Paenibacillus larvae. Environ Microbiol 16(5):1297–1309
Garcia-Gonzalez E, Muller S, Hertlein G, Heid N, Sussmuth RD, Genersch E (2014b) Biological effects of paenilamicin, a secondary metabolite antibiotic produced by the honey bee pathogenic bacterium Paenibacillus larvae. Microbiologyopen 3(5):642–656. https://doi.org/10.1002/mbo3.195
Grady EN, MacDonald J, Liu L, Richman A, Yuan ZC (2016) Current knowledge and perspectives of Paenibacillus: a review. Microb Cell Factories 15(1):203. https://doi.org/10.1186/s12934-016-0603-7
Gray EJ, Di Falco M, Souleimanov A, Smith DL (2006a) Proteomic analysis of the bacteriocin thuricin 17 produced by Bacillus thuringiensis NEB17. FEMS Microbiol Lett 255(1):27–32. https://doi.org/10.1111/j.1574-6968.2005.00054.x
Gray EJ, Lee KD, Souleimanov AM, Di Falco MR, Zhou X, Ly A, Charles TC, Driscoll BT, Smith DL (2006b) A novel bacteriocin, thuricin 17, produced by plant growth promoting rhizobacteria strain Bacillus thuringiensis NEB17: isolation and classification. J Appl Microbiol 100(3):545–554. https://doi.org/10.1111/j.1365-2672.2006.02822.x
Guo Y, Huang E, Yuan C, Zhang L, Yousef AE (2012) Isolation of a Paenibacillus sp. strain and structural elucidation of its broad-spectrum lipopeptide antibiotic. Appl Environ Microbiol 78(9):3156–3165. https://doi.org/10.1128/AEM.07782-11
Gustafson K, Roman M, Fenical W (1989) The macrolactins, a novel class of antiviral and cytotoxic macrolides from a deep-sea marine bacterium. J Am Chem Soc 111(19):7519–7524
He Z, Kisla D, Zhang L, Yuan C, Green-Church KB, Yousef AE (2007) Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic and polymyxin. Appl Environ Microbiol 73(1):168–178. https://doi.org/10.1128/aem.02023-06
He Z, Yuan C, Zhang L, Yousef AE (2008) N-terminal acetylation in paenibacillin, a novel lantibiotic. FEBS Lett 582(18):2787–2792. https://doi.org/10.1016/j.febslet.2008.07.008
Helfrich EJ, Piel J (2016) Biosynthesis of polyketides by trans-AT polyketide synthases. Nat Prod Rep 33(2):231–316. https://doi.org/10.1039/c5np00125k
Hertweck C (2009) The biosynthetic logic of polyketide diversity. Angew Chem Int Ed Eng 48(26):4688–4716. https://doi.org/10.1002/anie.200806121
Hinchliffe P, Yang QE, Portal E, Young T, Li H, Tooke CL, Carvalho MJ, Paterson NG, Brem J, Niumsup PR, Tansawai U, Lei L, Li M, Shen Z, Wang Y, Schofield CJ, Mulholland AJ, Shen J, Fey N, Walsh TR, Spencer J (2017) Insights into the mechanistic basis of plasmid-mediated colistin resistance from crystal structures of the catalytic domain of MCR-1. Sci Rep 7:39392. https://doi.org/10.1038/srep39392
Holland IB, Roberts CF (1964) Some properties of a new bacteriocin formed by Bacillus megaterium. J Gen Microbiol 35:271–285. https://doi.org/10.1099/00221287-35-2-271
Huang E, Yousef AE (2012) Draft genome sequence of Paenibacillus polymyxa OSY-DF, which coproduces a lantibiotic, paenibacillin, and polymyxin E1. J Bacteriol 194(17):4739–4740
Huang E, Yousef AE (2014) The lipopeptide antibiotic paenibacterin binds to the bacterial outer membrane and exerts bactericidal activity through cytoplasmic membrane damage. Appl Environ Microbiol 80(9):2700–2704. https://doi.org/10.1128/AEM.03775-13
Huang E, Yousef AE (2015) Biosynthesis of paenibacillin, a lantibiotic with N-terminal acetylation, by Paenibacillus polymyxa. Microbiol Res 181:15–21. https://doi.org/10.1016/j.micres.2015.08.001
Huang T, Geng H, Miyyapuram VR, Sit CS, Vederas JC, Nakano MM (2009) Isolation of a variant of subtilosin A with hemolytic activity. J Bacteriol 191(18):5690–5696. https://doi.org/10.1128/jb.00541-09
Huang E, Guo Y, Yousef AE (2014) Biosynthesis of the new broad-spectrum lipopeptide antibiotic paenibacterin in Paenibacillus thiaminolyticus OSY-SE. Res Microbiol 165(3):243–251. https://doi.org/10.1016/j.resmic.2014.02.002
Hyronimus B, Le Marrec C, Urdaci MC (1998) Coagulin, a bacteriocin-like inhibitory substance produced by Bacillus coagulans I4. J Appl Microbiol 85(1):42–50
Jung M, Lee S, Kim H (2000) Recent studies on natural products as anti-HIV agents. Curr Med Chem 7(6):649–661
Kalyon B, Helaly SE, Scholz R, Nachtigall J, Vater J, Borriss R, Sussmuth RD (2011) Plantazolicin A and B: structure elucidation of ribosomally synthesized thiazole/oxazole peptides from Bacillus amyloliquefaciens FZB42. Org Lett 13(12):2996–2999. https://doi.org/10.1021/ol200809m
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(4):881–888. https://doi.org/10.1111/j.1365-2672.2004.02513.x
Kato T, Shoji J (1976) The amino acid sequence of octapeptin C1 (333-25) studies on antibiotics from the genus Bacillus. XIX. J Antibiot (Tokyo) 29(12):1339–1340
Kato T, Sakazaki R, Hinoo H, Shoji J (1979) The structures of tridecaptins B and C (studies on antibiotics from the genus Bacillus. XXV). J Antibiot (Tokyo) 32(4):305–312
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 cross-links: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry 43(12):3385–3395. https://doi.org/10.1021/bi0359527
Kenig M, Abraham EP (1976) Antimicrobial activities and antagonists of bacilysin and anticapsin. J Gen Microbiol 94(1):37–45. https://doi.org/10.1099/00221287-94-1-37
Kiss A, Baliko G, Csorba A, Chuluunbaatar T, Medzihradszky KF, Alfoldi L (2008) Cloning and characterization of the DNA region responsible for Megacin A-216 production in Bacillus megaterium 216. J Bacteriol 190(19):6448–6457. https://doi.org/10.1128/jb.00557-08
Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94(11):1259–1266. https://doi.org/10.1094/phyto.2004.94.11.1259
Konz D, Klens A, Schorgendorfer K, Marahiel MA (1997) The bacitracin biosynthesis operon of Bacillus licheniformis ATCC 10716: molecular characterization of three multi-modular peptide synthetases. Chem Biol 4, 927(12):–937. https://doi.org/10.1016/S1074-5521(97)90301-X
Koumoutsi A, Chen XH, 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(4):1084–1096
Lawton EM, Ross RP, Hill C, Cotter PD (2007) Two-peptide lantibiotics: a medical perspective. Mini-Rev Med Chem 7(12):1236–1247
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 I(4). Appl Environ Microbiol 66(12):5213–5220
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(8):4577–4584. https://doi.org/10.1128/aem.71.8.4577-4584.2005
Lee H, Churey JJ, Worobo RW (2009a) Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiol Lett 299(2):205–213. https://doi.org/10.1111/j.1574-6968.2009.01749.x
Lee KD, Gray EJ, Mabood F, Jung WJ, Charles T, Clark SR, Ly A, Souleimanov A, Zhou X, Smith DL (2009b) The class IId bacteriocin thuricin-17 increases plant growth. Planta 229(4):747–755. https://doi.org/10.1007/s00425-008-0870-6
Lee SH, Cho YE, Park SH, Balaraju K, Park JW, Lee SW, Park K (2013) An antibiotic fusaricidin: a cyclic depsipeptide from Paenibacillus polymyxa E681 induces systemic resistance against Phytophthora blight of red-pepper. Phytoparasitica 41(1):49–58. https://doi.org/10.1007/s12600-012-0263-z
Li W, Tang XX, Yan X, Wu Z, Yi ZW, Fang MJ, Su X, Qiu YK (2016) A new macrolactin antibiotic from deep sea-derived bacteria Bacillus subtilis B5. Nat Prod Res 30:2777–2782. https://doi.org/10.1080/14786419.2016.1155576
Li YX, Zhong Z, Hou P, Zhang WP, Qian PY (2018a) Resistance to nonribosomal peptide antibiotics mediated by D-stereospecific peptidases. Nat Chem Biol 14(4):381–387. https://doi.org/10.1038/s41589-018-0009-4
Li YX, Zhong Z, Zhang WP, Qian PY (2018b) Discovery of cationic nonribosomal peptides as Gram-negative antibiotics through global genome mining. Nat Commun 9. https://doi.org/10.1038/s41467-018-05781-6
Liu R-F, Zhang D-J, Li Y-G, Tao L-M, Tian L (2010) A new antifungal cyclic lipopeptide from Bacillus marinus B-9987. Helv Chim Acta 93(12):2419–2425. https://doi.org/10.1002/hlca.201000094
Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16(2):161–168. https://doi.org/10.1016/s1473-3099(15)00424-7
Lohans CT, Huang Z, van Belkum MJ, Giroud M, Sit CS, Steels EM, Zheng J, Whittal RM, McMullen LM, Vederas JC (2012) Structural characterization of the highly cyclized lantibiotic paenicidin A via a partial desulfurization/reduction strategy. J Am Chem Soc 134(48):19540–19543. https://doi.org/10.1021/ja3089229
Lohans CT, van Belkum MJ, Cochrane SA, Huang Z, Sit CS, McMullen LM, Vederas JC (2014) Biochemical, structural, and genetic characterization of tridecaptin A(1), an antagonist of Campylobacter jejuni. Chembiochem 15(2):243–249. https://doi.org/10.1002/cbic.201300595
Luo C, Liu X, Zhou X, Guo J, Truong J, Wang X, Zhou H, Li X, Chen Z (2015) Unusual biosynthesis and structure of locillomycins from Bacillus subtilis 916. Appl Environ Microbiol 81(19):6601–6609. https://doi.org/10.1128/aem.01639-15
Ma Z, Wang N, Hu J, Wang S (2012) Isolation and characterization of a new iturinic lipopeptide, mojavensin A produced by a marine-derived bacterium Bacillus mojavensis B0621A. J Antibiot 65(6):317–322 http://www.nature.com/ja/journal/v65/n6/suppinfo/ja201219s1.html
Maget-Dana R, Thimon L, Peypoux F, Ptak M (1992) Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74(12):1047–1051
Martin NI, Hu H, Moake MM, Churey JJ, Whittal R, Worobo RW, Vederas JC (2003) Isolation, structural characterization, and properties of mattacin (polymyxin M), a cyclic peptide antibiotic produced by Paenibacillus kobensis M. J Biol Chem 278(15):13124–13132. https://doi.org/10.1074/jbc.M212364200
Marx R, Stein T, Entian KD, Glaser SJ (2001) 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(6):501–506
McClerren AL, Cooper LE, Quan C, Thomas PM, Kelleher NL, van der Donk WA (2006) Discovery and in vitro biosynthesis of haloduracin, a two-component lantibiotic. Proc Natl Acad Sci U S A 103(46):17243–17248. https://doi.org/10.1073/pnas.0606088103
Meyers E, Parker WL, Brown WE (1976) A nomenclature proposal for the octapeptin antibiotics. J Antibiot (Tokyo) 29(11):1241–1242
Muller S, Garcia-Gonzalez E, Mainz A, Hertlein G, Heid NC, Mosker E, van den Elst H, Overkleeft HS, Genersch E, Sussmuth RD (2014) Paenilamicin: structure and biosynthesis of a hybrid nonribosomal peptide/polyketide antibiotic from the bee pathogen Paenibacillus larvae. Angew Chem Int Ed Eng 53(40):10821–10825. https://doi.org/10.1002/anie.201404572
Nihorimbere V, Ongena C, Cawoy H, Brostaux Y, Kakana P, Jourdan E, Thonart P (2010) Beneficial effects of Bacillus subtilis on field-grown tomato in Burundi: reduction of local Fusarium disease and growth promotion. Afr J Microbiol Res 4(11):1135–1142
Niu B, Vater J, Rueckert C, Blom J, Lehmann M, Ru JJ, Chen XH, Wang Q, Borriss R (2013) Polymyxin P is the active principle in suppressing phytopathogenic Erwinia spp. by the biocontrol rhizobacterium Paenibacillus polymyxa M-1. BMC Microbiol 13:137. https://doi.org/10.1186/1471-2180-13-137
O'Hagan D (1992) Biosynthesis of polyketide metabolites. Nat Prod Rep 9(5):447–479
Oman TJ, van der Donk WA (2009) Insights into the mode of action of the two-peptide lantibiotic haloduracin. ACS Chem Biol 4(10):865–874. https://doi.org/10.1021/cb900194x
Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16(3):115–125. https://doi.org/10.1016/j.tim.2007.12.009
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(4):1084–1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x
Orwa JA, Govaerts C, Busson R, Roets E, Van Schepdael A, Hoogmartens J (2001) Isolation and structural characterization of polymyxin B components. J Chromatogr A 912(2):369–373
Oscariz JC, Pisabarro AG (2000) Characterization and mechanism of action of cerein 7, a bacteriocin produced by Bacillus cereus Bc7. J Appl Microbiol 89(2):361–369
Oscariz JC, Lasa I, Pisabarro AG (1999) Detection and characterization of cerein 7, a new bacteriocin produced by Bacillus cereus with a broad spectrum of activity. FEMS Microbiol Lett 178(2):337–341
Oscariz JC, Cintas L, Holo H, Lasa I, Nes IF, Pisabarro AG (2006) Purification and sequencing of cerein 7B, a novel bacteriocin produced by Bacillus cereus Bc7. FEMS Microbiol Lett 254(1):108–115. https://doi.org/10.1111/j.1574-6968.2005.00009.x
Patel H, Tscheka C, Edwards K, Karlsson G, Heerklotz H (2011) All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713. Biochim Biophys Acta 1808(8):2000–2008. https://doi.org/10.1016/j.bbamem.2011.04.008
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(4):636–645
Pattnaik P, Grover S, Batish VK (2005) Effect of environmental factors on production of lichenin, a chromosomally encoded bacteriocin-like compound produced by Bacillus licheniformis 26L-10/3RA. Microbiol Res 160(2):213–218
Pichard B, Larue JP, Thouvenot D (1995) Gavaserin and saltavalin, new peptide antibiotics produced by Bacillus polymyxa. FEMS Microbiol Lett 133(3):215–218
Pirri G, Giuliani A, Nicoletto SF, Pizzuto L, Rinaldi AC (2009) Lipopeptides as anti-infectives: a practical perspective. Cent Eur J Biol 4(3):258–273. https://doi.org/10.2478/s11535-009-0031-3
Qi G, Zhu F, Du P, Yang X, Qiu D, Yu Z, Chen J, Zhao X (2010) Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway. Peptides 31(11):1978–1986. https://doi.org/10.1016/j.peptides.2010.08.003
Qian CD, Liu TZ, Zhou SL, Ding R, Zhao WP, Li O, Wu XC (2012a) Identification and functional analysis of gene cluster involvement in biosynthesis of the cyclic lipopeptide antibiotic pelgipeptin produced by Paenibacillus elgii. BMC Microbiol 12:197. https://doi.org/10.1186/1471-2180-12-197
Qian CD, Wu XC, Teng Y, Zhao WP, Li O, Fang SG, Huang ZH, Gao HC (2012b) Battacin (Octapeptin B5), a new cyclic lipopeptide antibiotic from Paenibacillus tianmuensis active against multidrug-resistant Gram-negative bacteria. Antimicrob Agents Chemother 56(3):1458–1465. https://doi.org/10.1128/aac.05580-11
Ramarathnam R, Bo S, Chen Y, Fernando WG, 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(7):901–911. https://doi.org/10.1139/w07-049
Raza W, Yang W, Shen QR (2008) Paenibacillus polymyxa: antibiotics, hydrolytic enzymes and hazard assessment. J Plant Pathol 90(3):419–430
Raza W, Yang XM, Wu HS, Wang Y, Xu YC, Shen QR (2009) Isolation and characterisation of fusaricidin-type compound-producing strain of Paenibacillus polymyxa SQR-21 active against Fusarium oxysporum f. sp nevium. Eur J Plant Pathol 125(3):471–483. https://doi.org/10.1007/s10658-009-9496-1
Righi E, Giacomazzi CG, Bassetti M, Bisio F, Soro O, McDermott JL, Varnier OE, Ratto S, Viscoli C (2007) Soft-tissue infection with Absidia corymbifera and kidney complications in an AIDS patient. Med Mycol 45(7):637–640. https://doi.org/10.1080/13693780701435358
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(4):430–440. https://doi.org/10.1094/mpmi-20-4-0430
Romero-Tabarez M, Jansen R, Sylla M, Lunsdorf H, Haussler 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(5):1701–1709. https://doi.org/10.1128/AAC.50.5.1701-1709.2006
Rybakova D, Wetzlinger U, Muller H, Berg G (2015) Complete genome sequence of Paenibacillus polymyxa strain Sb3-1, a soilborne bacterium with antagonistic activity toward plant pathogens. Genome Announc 3(2). https://doi.org/10.1128/genomeA.00052-15
Schneider K, Chen XH, Vater J, Franke P, Nicholson G, Borriss R, Sussmuth RD (2007) Macrolactin is the polyketide biosynthesis product of the pks2 cluster of Bacillus amyloliquefaciens FZB42. J Nat Prod 70(9):1417–1423. https://doi.org/10.1021/np070070k
Scholz R, Vater J, Budiharjo A, Wang Z, He Y, Dietel K, Schwecke T, Herfort S, Lasch P, Borriss R (2014) Amylocyclicin, a novel circular bacteriocin produced by Bacillus amyloliquefaciens FZB42. J Bacteriol 196(10):1842–1852. https://doi.org/10.1128/jb.01474-14
Sebei S, Zendo T, Boudabous A, Nakayama J, Sonomoto K (2007) Characterization, N-terminal sequencing and classification of cerein MRX1, a novel bacteriocin purified from a newly isolated bacterium: Bacillus cereus MRX1. J Appl Microbiol 103(5):1621–1631. https://doi.org/10.1111/j.1365-2672.2007.03395.x
Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7(2):285–295
Shoji J, Kato T, Sakazaki R (1976) The total structure of cerexin A (studies on antibiotics from the genus Bacillus. XVI). J Antibiot (Tokyo) 29(12):1268–1274
Shoji J, Kato T, Hinoo H (1977) The structures of two new polymyxin group antibiotics. J Antibiot (Tokyo) 30(5):427–429
Singh AK, Ghodke I, Chhatpar HS (2009) Pesticide tolerance of Paenibacillus sp. D1 and its chitinase. J Environ Manag 91(2):358–362. https://doi.org/10.1016/j.jenvman.2009.09.001
Sogn JA (1976) Structure of the peptide antibiotic polypeptin. J Med Chem 19(10):1228–1231
Sood S, Steinmetz H, Beims H, Mohr KI, Stadler M, Djukic M, von der Ohe W, Steinert M, Daniel R, Muller R (2014) Paenilarvins: iturin family lipopeptides from the honey bee pathogen Paenibacillus larvae. Chembiochem 15(13):1947–1955. https://doi.org/10.1002/cbic.201402139
Stansly PG, Shepherd RG, White HJ (1947) Polymyxin: a new chemotherapeutic agent. Bull Johns Hopkins Hosp 81(1):43–54
Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56(4):845–857. https://doi.org/10.1111/j.1365-2958.2005.04587.x
Stein T, Dusterhus S, Stroh A, Entian KD (2004) Subtilosin production by two Bacillus subtilis subspecies and variance of the sbo-alb cluster. Appl Environ Microbiol 70(4):2349–2353
Stern NJ, Svetoch EA, Urakov NN, Eruslanov BV, Volodina LI, Kovalev YN, Kudryavtseva TY, Perelygin VV, Pokhilenko VD, Levchuk VP, Borzenkov VN (2013) Bacteriocins and novel bacterial strains. United States patent application US 13/533,037
Sumi CD, Yang BW, Yeo IC, Hahm YT (2015) Antimicrobial peptides of the genus Bacillus: a new era for antibiotics. Can J Microbiol 61(2):93–103. https://doi.org/10.1139/cjm-2014-0613
Sun J, Zhang H, Liu YH, Feng Y (2018) Towards understanding MCR-like colistin resistance. Trends Microbiol 26:794–808. https://doi.org/10.1016/j.tim.2018.02.006
Svetoch EA, Stern NJ, Eruslanov BV, Kovalev YN, Volodina LI, Perelygin VV, Mitsevich EV, Mitsevich IP, Pokhilenko VD, Borzenkov VN, Levchuk VP, Svetoch OE, Kudriavtseva TY (2005) Isolation of Bacillus circulans and Paenibacillus polymyxa strains inhibitory to Campylobacter jejuni and characterization of associated bacteriocins. J Food Prot 68(1):11–17
Tapi A, Chollet-Imbert M, Scherens B, Jacques P (2010) New approach for the detection of non-ribosomal peptide synthetase genes in Bacillus strains by polymerase chain reaction. Appl Microbiol Biotechnol 85(5):1521–1531. https://doi.org/10.1007/s00253-009-2176-4
Teng Y, Zhao W, Qian C, Li O, Zhu L, Wu X (2012) Gene cluster analysis for the biosynthesis of elgicins, novel lantibiotics produced by Paenibacillus elgii B69. BMC Microbiol 12:45. https://doi.org/10.1186/1471-2180-12-45
Umezawa H, Aoyagi T, Nishikiori T, Okuyama A, Yamagishi Y, Hamada M, Takeuchi T (1986) Plipastatins: new inhibitors of phospholipase A2, produced by Bacillus cereus BMG302-fF67. I. Taxonomy, production, isolation and preliminary characterization. J Antibiot (Tokyo) 39(6):737–744
Vater J, Niu B, Dietel K, Borriss R (2015) Characterization of novel fusaricidins produced by Paenibacillus polymyxa-M1 using MALDI-TOF mass spectrometry. J Am Soc Mass Spectrom 26(9):1548–1558. https://doi.org/10.1007/s13361-015-1130-1
Velkov T, Thompson PE, Nation RL, Li J (2010) Structure–activity relationships of polymyxin antibiotics. J Med Chem 53(5):1898–1916. https://doi.org/10.1021/jm900999h
Velkov T, Gallardo-Godoy A, Swarbrick JD, Blaskovich MAT, Elliott AG, Han M, Thompson PE, Roberts KD, Huang JX, Becker B, Butler MS, Lash LH, Henriques ST, Nation RL, Sivanesan S, Sani MA, Separovic F, Mertens H, Bulach D, Seemann T, Owen J, Li J, Cooper MA (2018) Structure, function, and biosynthetic origin of octapeptin antibiotics active against extensively drug-resistant gram-negative bacteria. Cell Chem Biol 25(4):380–391 e5. https://doi.org/10.1016/j.chembiol.2018.01.005
Von Tersch MA, Carlton BC (1983) Bacteriocin from Bacillus megaterium ATCC 19213: comparative studies with megacin A-216. J Bacteriol 155(2):866–871
Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303(5665):1805–1810. https://doi.org/10.1126/science.1094318
Willey JM, van der Donk WA (2007) Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61:477–501. https://doi.org/10.1146/annurev.micro.61.080706.093501
Wu XC, Shen XB, Ding R, Qian CD, Fang HH, Li O (2010) Isolation and partial characterization of antibiotics produced by Paenibacillus elgii B69. FEMS Microbiol Lett 310(1):32–38. https://doi.org/10.1111/j.1574-6968.2010.02040.x
Wu XC, Qian CD, Fang HH, Wen YP, Zhou JY, Zhan ZJ, Ding R, Li O, Gao H (2011) Paenimacrolidin, a novel macrolide antibiotic from Paenibacillus sp. F6-B70 active against methicillin-resistant Staphylococcus aureus. Microb Biotechnol 4(4):491–502. https://doi.org/10.1111/j.1751-7915.2010.00201.x
Wu L, Wu H, Chen L, Yu X, Borriss R, Gao X (2015) Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against Xanthomonas oryzae rice pathogens. Sci Rep 5:12975. https://doi.org/10.1038/srep12975
Yousef A. E, Yaoqi G, Huang En (2013) Biosynthesis of paenibacillin. World Intellectual Property Organization WO/2013/180699
Yu WB, Ye BC (2016) High-level iron mitigates fusaricidin-induced membrane damage and reduces membrane fluidity leading to enhanced drug resistance in Bacillus subtilis. J Basic Microbiol 56(5):502–509. https://doi.org/10.1002/jobm.201500291
Zarei I (2012) Biosynthesis of bacitracin in stirred fermenter by Bacillus licheniformis using defatted oil seed cakes as substrate. Mod Appl Sci 6(2):30
Zhang B, Dong C, Shang Q, Han Y, Li P (2013) New insights into membrane-active action in plasma membrane of fungal hyphae by the lipopeptide antibiotic bacillomycin L. Biochim Biophys Acta 1828(9):2230–2237. https://doi.org/10.1016/j.bbamem.2013.05.033
Zheng G, Hehn R, Zuber P (2000) Mutational analysis of the sbo-alb locus of Bacillus subtilis: identification of genes required for subtilosin production and immunity. J Bacteriol 182(11):3266–3273
Zimmerman SB, Schwartz CD, Monaghan RL, Pelak BA, Weissberger B, Gilfillan EC, Mochales S, Hernandez S, Currie SA, Tejera E, Stapley EO (1987) Difficidin and oxydifficidin: novel broad spectrum antibacterial antibiotics produced by Bacillus subtilis. I. Production, taxonomy and antibacterial activity. J Antibiot (Tokyo) 40(12):1677–1681
Funding
This work was supported by grants from the Consortium de recherche et innovations en bioprocédés industriels au Québec (CRIBIQ) and the Natural Sciences and Engineering Research Council of Canada (NSERC).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Olishevska, S., Nickzad, A. & Déziel, E. Bacillus and Paenibacillus secreted polyketides and peptides involved in controlling human and plant pathogens. Appl Microbiol Biotechnol 103, 1189–1215 (2019). https://doi.org/10.1007/s00253-018-9541-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9541-0