Advertisement

Secondary Metabolites of the Plant Growth Promoting Model Rhizobacterium Bacillus velezensis FZB42 Are Involved in Direct Suppression of Plant Pathogens and in Stimulation of Plant-Induced Systemic Resistance

  • Rainer BorrissEmail author
  • Huijun Wu
  • Xuewen Gao
Chapter

Abstract

Thirteen gene clusters involved in non-ribosomal and ribosomal synthesis of secondary metabolites with putative antimicrobial action have been identified within the genome of FZB42, the model for Gram-positive biocontrol strains. These gene clusters cover around ten percentage of the whole genome. Antimicrobial compounds not only suppress growth of plant pathogenic bacteria and fungi but could also stimulate induced systemic response (ISR) in plants. Recently, it has been found that besides secondary metabolites also a blend of volatile organic compounds (VOCs) is involved in the biocontrol effect exerted by FZB42 against plant pathogens suggesting complexity of biocontrol function. Cyclic lipopeptides and volatiles produced by plant-associated bacilli trigger pathways of induced systemic resistance (ISR), which protect plants against attacks of pathogenic microbes, viruses, and nematodes. Stimulation of ISR by bacterial metabolites is likely the main mechanism responsible for biocontrol action of FZB42.

Keywords

Bacillus Secondary metabolites Biological control ISR Phytopathogens 

References

  1. Allard-Massicotte R, Tessier L, Lecuyer F, Lakshmanan V, Lucier JF, Garneau D et al (2017) Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. MBio 7:e01664–e01616Google Scholar
  2. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS et al (2013) Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 30(1):108–160.  https://doi.org/10.1039/c2np20085f CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75.  https://doi.org/10.1186/1471-2164-9–75 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Belitsky B, Sonenshein A (2013) Genome-wide identification of Bacillus subtilis CodY-binding sites at single-nucleotide resolution. Proc Natl Acad Sci U S A 110:7026–7031.  https://doi.org/10.1073/pnas.1300428110 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blom J, Rueckert C, Niu B, Wang Q, Borriss R (2012) The complete genome of Bacillus amyloliquefaciens subsp. plantarum CAU B946 contains a gene cluster for nonribosomal synthesis of iturin a. J Bacteriol 194:1845–1846CrossRefGoogle Scholar
  7. Bock H (1552) De stirpium, earum, quae in Germania nostra nascuntur commentariorum libri tres. Wendelin Rihel, Strassburg (First Latin edition)Google Scholar
  8. Borriss R (2011) Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Heidelberg/Dordrecht/London/New York, pp 41–76CrossRefGoogle Scholar
  9. Borriss R (2015) Towards a new generation of commercial microbial disease control and plant growth promotion products. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer, Germany, pp 329–337.  https://doi.org/10.1007/978-3-319-08575-3 CrossRefGoogle Scholar
  10. Borriss R (2016) Phytostimulation and biocontrol by the plant-associated Bacillus amyloliquefaciens FZB42: an update. In: Islam MT et al (eds) Bacilli and agrobiotechnology. Springer International Publishing AG, Berlin, pp 163–184CrossRefGoogle Scholar
  11. Borriss R, Chen XH, Rueckert C, Blom J, Becker A, Baumgarth B, Fan B, Pukall R, Schumann P, Sproer C, Junge H, Vater J, Pühler A, Klenk HP (2011) Relationship of Bacillus amyloliquefaciens clades associated with strains DSM 7T and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on their discriminating complete genome sequences. Int J Syst Evol Microbiol 61:1786–1801CrossRefGoogle Scholar
  12. Borriss R, Danchin A, Harwood CR, Médigue C, Rocha EPC, Sekowska A, Vallenet D (2018) Bacillus subtilis, the model gram-positive bacterium: 20 years of annotation refinement. Microb Biotechnol 11(1):3–17.  https://doi.org/10.1111/1751-7915.13043 CrossRefPubMedGoogle Scholar
  13. Burkhart BJ, Hudson GA, Dunbar KL, Mitchell DA (2015) A prevalent peptide-binding domain guides ribosomal natural product biosynthesis. Nat Chem Biol 11(8):564–570.  https://doi.org/10.1038/nchembio.1856 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Butcher BG, Helmann JD (2006) Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol Microbiol 60:765–782CrossRefGoogle Scholar
  15. 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):1506–9CrossRefGoogle Scholar
  16. Chatterjee S, Chatterjee DK, Lad SJ, Phansalkar MS, Rupp RH, Ganguli BN, Fehlhaber HW, Kogler H (1992) Mersacidin, a new antibiotic from Bacillus: fermentation, isolation, purification and chemical characterization. J Antibiot 45:832–838CrossRefGoogle Scholar
  17. Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Süssmuth R, Borriss R (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol 188:4024–4036CrossRefGoogle Scholar
  18. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K et al (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014CrossRefGoogle Scholar
  19. Chen XH, Scholz R, Borriss M, Junge H, Mögel G, Kunz S, Borriss R (2009a) Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140:38–44CrossRefGoogle Scholar
  20. Chen XH, Koumoutsi A, Scholz R, Borriss R (2009b) More than anticipated – production of antibiotics and other secondary metabolites by Bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol 16:14–24CrossRefGoogle Scholar
  21. Chowdhury SP, Dietel K, Rändler M, Schmid M, Junge H, Borriss R et al (2013) Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS One 8(7):e68818.  https://doi.org/10.1371/journal.pone.0068818 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chowdhury SP, Uhl J, Grosch R, Alquéres S, Pittroff S, Dietel K et al (2015a) Cyclic lipopeptides of Bacillus amyloliquefaciens FZB42 subsp. plantarum colonizing the lettuce rhizosphere enhance plant defence responses towards the bottom rot pathogen Rhizoctonia solani. Mol Plant-Microbe Interact (9):984–995.  https://doi.org/10.1094/MPMI-03-15-0066-R CrossRefGoogle Scholar
  23. Chowdhury SP, Hartmann A, Gao X, Borriss R (2015b) Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review. Front Microbiol 6:780.  https://doi.org/10.3389/fmicb.2015.00780 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Debois D, Jourdan E, Smargiasso N, Thonart P, de Pauw E, Ongena M (2014) Spatiotemporal monitoring of the antibiome secreted by Bacillus biofilms on plant roots using MALDI mass spectrometry imaging. Anal Chem 86:4431–4438.  https://doi.org/10.1021/ac500290s CrossRefPubMedGoogle Scholar
  25. Doornbos RF, van Loon LC, Bakker PA (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243CrossRefGoogle Scholar
  26. Duitman EH, Hamoen LW, Rembold M, Venema G, Seitz H, Saenger W, Bernhard F, Reinhardt R, Schmidt M, Ullrich C, Stein T, Leenders F, Vater J (1999) The mycosubtilin synthetase of Bacillus subtilis ATCC6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc Natl Acad Sci U S A 96(23):13294–13299CrossRefGoogle Scholar
  27. Dunlap C, Kim SJ, Kwon SW, Rooney A (2016) Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens, Bacillus methylotrophicus, Bacillus amyloliquefaciens subsp. plantarum and ‘Bacillus oryzicola’ are later heterotypic synonyms of Bacillus velezensis based on phylogenomics. Int J Syst Evol Microbiol 66:1212–1217.  https://doi.org/10.1099/ijsem.0.000858 CrossRefPubMedGoogle Scholar
  28. Ebel J, Scheel D (1997) Signals in host–parasite interactions. Springer, Berlin/HeidelbergCrossRefGoogle Scholar
  29. Erlacher A, Cardinale M, Grosch R, Grube M, Berg G (2014) The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome. Front Microbiol 5:175.  https://doi.org/10.3389/fmicb.2014.00175 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fan B, Blom J, Klenk HP, Borriss R (2017) Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an “operational group B. amyloliquefaciens” within the B. subtilis species complex. Front Microbiol 8:22.  https://doi.org/10.3389/fmicb.2017.00022 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gong W, Wang J, Chen Z, Xia B, Lu G (2011) Solution structure of LCI, a novel antimicrobial peptide from Bacillus subtilis. Biochemistry 50(18):3621–3627.  https://doi.org/10.1021/bi200123w CrossRefPubMedGoogle Scholar
  32. 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 111:7519–7524CrossRefGoogle Scholar
  33. Hao HT, Zhao X, Shang QH, Wang Y, Guo ZH, Zhang YB et al (2016) Comparative digital gene expression analysis of the Arabidopsis response to volatiles emitted by Bacillus amyloliquefaciens. PLoS One 11(8):0158621.  https://doi.org/10.1371/journal.pone.0158621 CrossRefGoogle Scholar
  34. He P, Hao K, Blom J, Rückert C, Vater J, Mao Z, Wu Y, Hou M, He P, He Y, Borriss R (2012) Genome sequence of the plant growth promoting strain Bacillus amyloliquefaciens subsp. plantarum B9601-Y2 and expression of mersacidin and other secondary metabolites. J Biotechnol 164(2):281–291.  https://doi.org/10.1016/j.jbiotec.2012.12.014 CrossRefPubMedGoogle Scholar
  35. Herzner AM, Dischinger J, Szekat C, Josten M, Schmitz S, Yakéléba A et al (2011) Expression of the lantibiotic mersacidin in Bacillus amyloliquefaciens FZB42. PLoS One 6(7):e22389.  https://doi.org/10.1371/journal.pone.0022389 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Idris EES, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant-Microbe Interact 20:619–626.  https://doi.org/10.1094/MPMI-20-6-0619 CrossRefPubMedGoogle Scholar
  37. Jacques P (2011) Surfactin and other Lipopeptides from Bacillus spp. In: Soberón-Chávez G (ed) Biosurfactants. Microbiology monographs, vol 20. Springer, Berlin/HeidelbergGoogle Scholar
  38. Kalyon B, Helaly SE, Scholz R, Nachtigall J, Vater J, Borriss R, Süssmuth RD (2011) Plantazolicin a and B: structure of ribosomally synthesized thiazole/oxazole peptides from Bacillus amyloliquefaciens FZB42. Org Lett 13:2996–2999.  https://doi.org/10.1021/ol200809m CrossRefPubMedGoogle Scholar
  39. Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franke P et al (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.  https://doi.org/10.1128/JB.186.4.1084-1096.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Koumoutsi A, Chen XH, Vater J, Borriss R, Deg U, Ycz E (2007) Positively regulate the synthesis of bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl Environ Microbiol 73:6953–6964CrossRefGoogle Scholar
  41. Kovacs AT, Grau R, Pollitt EJG (2017) Surfing of bacterial droplets: Bacillus subtilis sliding revisited. Proc Natl Acad Sci U S A 114:E8802CrossRefGoogle Scholar
  42. Krebs B, Höding B, Kübart S, Workie MA, Junge H, Schmiedeknecht G, Bochow H, Hevesi M (1998) Use of Bacillus subtilis as biocontrol agent. I. Activities and characterization of Bacillus subtilis strains. J Plant Dis Prot 105:181–197. (in German)Google Scholar
  43. Lee SW, Mitchell DA, Markley AL, Hensler ME, Gonzalez D, Wohlrab A, Dorrestein PC, Nizet V, Dixon JE (2008) Discovery of a widely distributed toxin biosynthetic gene cluster. Proc Natl Acad Sci U S A 105(15):5879–5884CrossRefGoogle Scholar
  44. Liu J, Zhou T, He D, Li XZ, Wu H, Liu W, Gao X (2011) Functions of lipopeptides bacillomycin D and fengycin in antagonism of Bacillus amyloliquefaciens C06 towards Monilinia fructicola. J Mol Microbiol Biotechnol 20:43–52CrossRefGoogle Scholar
  45. Liu Z, Budiharjo A, Wang P, Shi H, Fang J, Borriss R et al (2013) The highly modified microcin peptide plantazolicin is associated with nematicidal activity of Bacillus amyloliquefaciens FZB42. Appl Microbiol Biotechnol 97:10081–10090.  https://doi.org/10.1007/s00253-013-5247-5 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Medema MH, Kottmann R, Yilmaz P, Cummings M, Biggins JB et al (2015) Minimum information about a biosynthetic gene cluster. Nat Chem Biol 11(9):625–631.  https://doi.org/10.1038/nchembio.1890 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Molohon KJ, Melby JO, Lee J, Evans BS, Dunbar KL, Bumpus SB et al (2011) Structure determination and interception of biosynthetic intermediates for the plantazolicin class of highly discriminating antibiotics. ACS Chem Biol 6:1307–1313.  https://doi.org/10.1021/cb200339d CrossRefPubMedPubMedCentralGoogle Scholar
  48. Molohon KJ, Blair PM, Park S, Doroghazi JR, Maxson T, Hershfield JR et al (2016) Plantazolicin is an ultra-narrow spectrum antibiotic that targets the Bacillus anthracis membrane. ACS Infect Dis 2(3):207–220CrossRefGoogle Scholar
  49. Müller S, Strack SN, Hoefer BC, Straight PD, Kearns DB, Kirby JR (2014) Bacillaene and sporulation protect Bacillus subtilis from predation by Myxococcus xanthus. Appl Environ Microbiol 80:5603–5610.  https://doi.org/10.1128/AEM.01621-14 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Moldenhauer J, Chen XH, Borriss R, Piel J (2007) Biosynthesis of the antibiotic bacillaene, the product of the giant polyketide SynthaseVomplex of the trans-AT family. Angew Chem Int Ed Engl 46(43):8195–7CrossRefGoogle Scholar
  51. Moldenhauer J, Götz DCG, Albert CR, Bischof SK, Schneider K, Süssmuth RD, Engeser M, Gross H, Bringmann G, Piel J (2010) The final steps of bacillaene biosynthesis in Bacillus amyloliquefaciens FZB42: direct evidence for beta gamma dehydration by a trans-acyltransferase polyketide synthase. Angew Chem Int Ed Engl 49(8):1465–7CrossRefGoogle Scholar
  52. Nakano C, Ozawa H, Akanuma G, Funa N, Horinouchi S (2009) Biosynthesis of aliphatic polyketides by type III polyketide synthase and methyltransferase in Bacillus subtilis. J Bacteriol 191(15):4916–4923.  https://doi.org/10.1128/JB.00407-09 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Nicholson WL (2008) The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2, 3-butandiol dehydrogenase. Appl Environ Microbiol 74:6832–6838CrossRefGoogle Scholar
  54. Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M (2012) Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79:176–191.  https://doi.org/10.1111/j.1574-6941.2011.01208.x CrossRefPubMedGoogle Scholar
  55. Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B et al (2007) Surfactin fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090CrossRefGoogle Scholar
  56. Patel PS, Huang S, Fisher S, Pirnik D, Aklonis C, Dean L et al (1995) Bacillaene, a novel inhibitor of prokaryotic protein synthesis produced by Bacillus subtilis: production, taxonomy isolation, physico-chemical characterization and biological activity. J Antibiot (Tokyo) 48:997–1003CrossRefGoogle Scholar
  57. Peipoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–563CrossRefGoogle Scholar
  58. Portalier R, Robert-Baudouy J, Stoeber F (1980) Regulation of Escherichia coli K-12 hexauronate system genes: exu regulon. J Bacteriol 143:1095–1107PubMedPubMedCentralGoogle Scholar
  59. Rahman A, Uddin W, Wenner NG (2015) Induced systemic resistance responses in perennial ryegrass against Magnaporthe oryzae elicited by semi-purified surfactin lipopeptides and live cells of Bacillus amyloliquefaciens. Mol Plant Pathol 16(6):546–558.  https://doi.org/10.1111/mpp.12209 CrossRefPubMedGoogle Scholar
  60. Romero-Tabarez M, Jansen B, Sylla M, Luensdorf H, Häussler S, Santosa DA et al (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 50:1701–1709CrossRefGoogle Scholar
  61. Rueckert C, Blom J, Chen XH, Reva O, Borriss R (2011) Genome sequence of Bacillus amyloliquefaciens type strain DSM7T reveals differences to plant-associated Bacillus amyloliquefaciens FZB42. J Biotechnol 155:78–85CrossRefGoogle Scholar
  62. Ryu C, Farag MA, Hu C, Reddy MS, Wei H, Pare PW et al (2003) Bacterial volatiles promote growth in Arabidopsis. PNAS 100:4927–4932CrossRefGoogle Scholar
  63. Schneider K, Chen XH, Vater J, Franke P, Nicholson G, Borriss R, Süssmuth RD (2007) Macrolactin is the polyketide biosynthesis product of the pks2 cluster of Bacillus amyloliquefaciens FZB42. J Nat Prod 70:1417–1423CrossRefGoogle Scholar
  64. Schnell N, Entian KD, Schneider U, Götz F, Zähner H, Kellner R, Jung G (1988) Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature 333:276–278.  https://doi.org/10.1038/333276a0 CrossRefPubMedGoogle Scholar
  65. Scholz R, Molohon KJ, Nachtigall J, Vater J, Markley AL, Süssmuth RD et al (2011) Plantazolicin, a novel microcin B17/streptolysin S-like natural product from Bacillus amyloliquefaciens FZB42. J Bacteriol 193:215–224.  https://doi.org/10.1128/JB.00784-10 CrossRefPubMedGoogle Scholar
  66. 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 196:1842–1852CrossRefGoogle Scholar
  67. Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285–295CrossRefGoogle Scholar
  68. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845–857CrossRefGoogle Scholar
  69. Stein T, Borchert S, Conrad B, Feesche J, Hofemeister B, Entian KD (2002) Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis. J Bacteriol 184(6):1703–1711CrossRefGoogle Scholar
  70. Straight PD, Fischbach MA, Walsh CT, Rudner DZ, Kolter R (2007) A singular enzymatic megacomplex from Bacillus subtilis. Proc Natl Acad Sci U S A 104:305–310.  https://doi.org/10.1073/pnas.0609073103 CrossRefPubMedGoogle Scholar
  71. Tahir HAS, Gu Q, Wu H, Niu Y, Huo R, Gao X (2017a) Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci Rep 7:40481CrossRefGoogle Scholar
  72. Tahir HAS, Gu Q, Wu H, Raza W, Safdar A, Huang Z, Rajer FU, Gao X (2017b) Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol 17(1):133.  https://doi.org/10.1186/s12870-017-1083-6 CrossRefPubMedPubMedCentralGoogle Scholar
  73. van Belkum MJ, Martin-Visscher LA, Vederas JC (2011) Structure and genetics of circular bacteriocins. Trends Microbiol 19:411–418.  https://doi.org/10.1016/j.tim.2011.04.004 CrossRefPubMedGoogle Scholar
  74. Vargas-Bautista C, Rahlwes K, Straight P (2014) Bacterial competition reveals differential regulation of the pks genes by Bacillus subtilis. J Bacteriol 196(4):717–728.  https://doi.org/10.1128/JB.01022-13 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303:1805–1810CrossRefGoogle Scholar
  76. Wilson KE, Flor JE, Schwartz RE, Joshua H, Smith JL, Pelak BA et al (1987) Difficidin and oxydifficidin: novel broad spectrum antibacterial antibiotics produced by Bacillus subtilis: II. Isolation and physico-chemical characterization. J Antibiot (Tokyo) 40:1682–1691CrossRefGoogle Scholar
  77. Wipat A, Harwood CR (1999) The Bacillus subtilis genome sequence: the molecular blueprint of a soil bacterium. FEMS Microbiol Ecol 28:1–9CrossRefGoogle Scholar
  78. Wu L, Wu H, Chen L, Xie S, Zang H, Borriss R, Gao XW (2014a) Bacilysin from Bacillus amyloliquefaciens FZB42 has specific bactericidal activity against harmful algal bloom species. Appl Environ Microbiol 80:7512–7520.  https://doi.org/10.1128/AEM.02605-14 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wu L, Wu H, Chen L, Lin L, Borriss R, Gao X (2014b) Bacilysin overproduction in Bacillus amyloliquefaciens FZB42 markerless derivative strains FZBREP and FZBSPA enhances antibacterial activity. Appl Microbiol Biotechnol 99(10):4255–4263.  https://doi.org/10.1007/s00253-014-6251-0 CrossRefPubMedGoogle Scholar
  80. Wu L, Wu HJ, Chen L, Yu XF, Borriss R, Gao XW (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 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wu G, Liu Y, Xu Y, Zhang G, Shen Q, Zhang R (2018) Exploring elicitors of the beneficial Rhizobacterium Bacillus amyloliquefaciens SQR9 to induce plant systemic resistance and their interactions with plant signaling pathways. Mol Plant Microbe Interact.  https://doi.org/10.1094/MPMI-11-17-0273-R CrossRefGoogle Scholar
  82. Yokota K, Hayakawa H (2015) Impact of antimicrobial lipopeptides from Bacillus sp. on suppression of Fusarium yellows of tatsoi. Microbes Environ 30:281–283CrossRefGoogle Scholar
  83. Yoo JS, Zheng CJ, Lee S, Kwak JH, Kim WG (2006) Macrolactin N, a new peptide deformylase inhibitor produced by Bacillus subtilis. Bioorg Med Chem Lett 16:4889–4489CrossRefGoogle Scholar
  84. Yu D, Xu F, Zeng J, Zhan J (2012) Type III polyketide synthases in natural product biosynthesis. UBMB Life 64(4):285–229CrossRefGoogle Scholar
  85. Zhang N, Yang D, Kendall JRA, Borriss R, Druzhinina IS, Kubicek CP, Shen Q, Zhang R (2016) Comparative genomic analysis of Bacillus amyloliquefaciens and Bacillus subtilis reveals evolutional traits for adaptation to plant-associated habitats. Front Microbiol 7:2039.  https://doi.org/10.3389/fmicb.2017.00022 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zhao H, Shao D, Jiang C, Shi J, Li Q, Huang Q, Rajoka MSR, Yang H, Jin M (2017) Biological activity of lipopeptides from Bacillus. Appl Microbiol Biotechnol 101(15):5951–5960.  https://doi.org/10.1007/s00253-017-8396-0 CrossRefPubMedGoogle Scholar
  87. Zweerink MM, Edison A (1987) Difficidin and oxydifficidin: novel broad spectrum antibacterial antibiotics produced by Bacillus subtilis. III. Mode of action of difficidin. J Antibiot (Tokyo) 40:1691–1692CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Institut für Biologie, Humboldt UniversitätBerlinGermany
  2. 2.Department of Plant Pathology, College of Plant ProtectionNanjing Agricultural UniversityNanjingPeople’s Republic of China
  3. 3.Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of EducationNanjingPeople’s Republic of China

Personalised recommendations