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Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides

Abstract

The whole organisms can be packaged as biopesticides, but secondary metabolites secreted by microorganisms can also have a wide range of biological activities that either protect the plant against pests and pathogens or act as plant growth promotors which can be beneficial for the agricultural crops. In this review, we have compiled information about the most important secondary metabolites of three important bacterial genera currently used in agriculture pest and disease management.

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References

  1. Abebe-Akele F, Tisa LS, Cooper VS, Hatcher PJ, Abebe E, Thomas WK (2015) Genome sequence and comparative analysis of a putative entomopathogenic Serratia isolated from Caenorhabditis briggsae. BMC Genomics 16:531

  2. 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

  3. Aliye N, Fininsa C, Hiskias Y (2008) Evaluation of rhizosphere bacterial antagonists for their potential to bioproject potato (Solanum tuberosum) against bacterial wilt (Ralstonia solanacearum). Biol Control 47:282–288

  4. Altena K, Guder A, Cramer C, Bierbaum G (2000) Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster. Appl Environ Microbiol 66:2565–2571

  5. 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:e83037

  6. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, Camarero JA, Campopiano DJ, Challis GL, Clardy J, Cotter PD, Craik DJ, Dawson M, Dittmann E, Donadio S, Dorrestein PC, Entian KD, Fischbach MA, Garavelli JS, Göransson U, Gruber CW, Haft DH, Hemscheidt TK, Hertweck C, Hill C, Horswill AR, Jaspars M, Kelly WL, Klinman JP, Kuipers OP, Link AJ, Liu W, Marahiel MA, Mitchell DA, Moll GN, Moore BS, Müller R, Nair SK, Nes IF, Norris GE, Olivera BM, Onaka H, Patchett ML, Piel J, Reaney MJ, Rebuffat S, Ross RP, Sahl HG, Schmidt EW, Selsted ME, Severinov K, Shen B, Sivonen K, Smith L, Stein T, Süssmuth RD, Tagg JR, Tang GL, Truman AW, Vederas JC, Walsh CT, Walton JD, Wenzel SC, Willey JM, van der Donk WA (2013) Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 30:108–160

  7. Banowetz GM, Azevedo MD, Armstrong DJ, Halgren AB, Mills DI (2008) Germination arrest factor (GAF): biological properties of a novel, naturally-occurring herbicide produced by selected isolates of rhizosphere bacteria. Biol Control 46:380–390

  8. Basi-Chipalu S, Dischinger J, Josten M, Szekat C, Zweynert A, Sahl HG, Bierbaum G (2015) Pseudomycoicidin, a class II lantibiotic from Bacillus pseudomycoides. Appl Environ Microbiol 81:3419–3429

  9. Bennett AJ, Whipps JM (2008) Beneficial microorganism survival on seed, roots and in rhizosphere soil following application to seed during durum priming. Biol Control 44:349–361

  10. Berg G (2000) Diversity of antifungal and plant-associated Serratia plymuthica strains. J Antimicrob Chemother 88:952–960

  11. Bierbaum G, Sahl HG (2009) Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol 10:2–18

  12. Blankenfeldt W (2013) The biosynthesis of phenazines. In: Chincholkar S, Thomashow L. (Eds.), Microbial Phenazines. Springer Berlin Heidelberg, pp 1–17.

  13. Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173:170–177

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

  15. 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, Germany, pp 41–76

  16. 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

  17. Borriss R, Chen XH, Rueckert C, Blom J, Becker A, Baumgarth B, Fan B, Pukall R, Schumann P, Spröer 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 61:1786–1801

  18. Breukink E, de Kruijff B (1999) The lantibiotic nisin, a special case or not? Biochim Biophys Acta 1462:223–234

  19. Brodhagen M, Paulsen I, Loper JE (2005) Reciprocal regulation of pyoluteorin production with membrane transporter gene expression in Pseudomonas fluorescens Pf-5. Appl Environ Microbiol 71:6900–6909

  20. Budzikiewicz H (2004) Siderophores of the Pseudomonadaceae sensu stricto (fluorescent and non-fluorescent Pseudomonas spp.). Prog Chem Org Nat Prod 87:81–237

  21. Butcher RA, Schroeder FC, Fischbach MA, Straight PD, Kolter R, Wash D, Clardy J (2007) The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc Natl Acad Sci U S A 104:1506–1509

  22. Calderón CE, deVicente A, Cazorla FM (2014) Role of 2-hexyl, 5-propylresorcinol production by Pseudomonas chlororaphis PCL1606 in the multitrophic interactions in the avocado rhizosphere during the biocontrol process. FEMS Microbiol Ecol 89:20–31

  23. Cazorla FM, Duckett SB, Bergström ET, Noreen S, Odijk R, Lugtenberg BJJ, Thomas-Oates JE, Bloemberg GV (2006) Biocontrol of avocado dematophora root rot by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Mol Plant-Microbe Interact 19:418–428

  24. 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 45:832–838

  25. Chehimi S, Delalande F, Sable 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

  26. Cheluvappa R (2014) Standardized chemical synthesis of Pseudomonas aeruginosa pyocyanin. MethodsX. 1:67–73

  27. Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Süssmuth RD, Borriss R (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol 188:4024–4036

  28. 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 140:38–44

  29. 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 16:14–24

  30. 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

  31. 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 subsp. entomocidus HD9. J Appl Microbiol 95:990–1000

  32. Chin-A-Woeng TFC, van den Broke D, de Voer G, van der Drift KM, Tuinman S, Thomas-Oates JE, Lugtenberg BJ, Bloemberg GV (2001a) Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted into the growth medium. Mol Plant-Microbe Interact 14:969–979

  33. Chin-A-Woeng TFC, Thomas-Oates JE, Lugtenberg BJ, Bloemberg GV (2001b) Introduction of the phzH gene of Pseudomonas chlororaphis PCL1391 extends the range of biocontrol ability of phenazine-1-carboxylic acid-producing Pseudomonas spp. strains. Mol Plant-Microbe Interact 14:1006–1015

  34. Choi S-K, Park S-Y, Kim R, Lee C-H, Kim JF, Park S-H (2008) Identification and functional analysis of the fusaricidin biosynthetic gene of Paenibacillus polymyxa E681. Biochem Biophys Res Commun 365:89–95

  35. 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 191:3350–3358

  36. Chowdhury SP, Dietel K, Rändler M, Schmid M, Junge H, Borriss R, Hartmann A, Grosch R (2013) Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS One:e68818

  37. Coulthurst SJ, Barnard AM, Salmond GP (2005) Regulation and biosynthesis of carbapenem antibiotics in bacteria. Nat Rev Microbiol 3:295–306

  38. Cruz DN, Perazella MA, Bellomo R, De Cal M, Polanco N, Corradi V, Lentini P, Nalesso F, Ueno T, Ranieri VM (2007) Effectiveness of polymyxin B-immobilized fiber column in sepsis: a systematic review. Crit Care 11:R47

  39. Darshan N, Manonmani HK (2015) Prodigiosin and its potential applications. J Food Sci Tech Mys 52:5393–5407

  40. de Souza JT, Weller DM, Raaijmakers JM (2003) Effect of 2,4-diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. Phytopathology 93:966–975

  41. Debois D, Jourdan E, Smargiasso N, Thonart P, de Pauw E, Ongena M (2014) Spatio temporal monitoring of the antibiome secreted by Bacillus biofilms on plant roots using MALDI mass spectrometry imaging. Anal Chem 86:4431–4438

  42. Dietrich LEP, Teal TK, Price-Whelan A, Newman DK (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science. 321:1203–1206

  43. Dilantha-Fernando WG, Ramarathnam R, Akkanas SK, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964

  44. 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 96:13294–13299

  45. Dwivedi D, Johri BN (2003) Antifungals from fluorescent pseudomonads: biosynthesis and regulation. Curr Sci 85:1693–1673

  46. Ehling-Schulz M, Vukov N, Schulz A, Shaheen R, Andersson M, Märtlbauer E, Scherer S (2005) Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl Environ Microbiol 71:105–113

  47. El-Sayed AK, Hothersall J, Thomas CM (2001) Quorum-sensing-dependent regulation of biosynthesis of the polyketide antibiotic mupirocin in Pseudomonas fluorescens NCIMB 10586. Microbiol. 147:2127–2139

  48. 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

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

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

  51. Fineran PC, Slater H, Everson L, Hughes K, Salmond GP (2005) Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol Microbiol 56:1495–1517

  52. Frankowski J, Lorito M, Scala F, Schmid R, Berg G, Bahl H (2001) Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch Microbiol 176:421–426

  53. Fuchs SW, Jaskolla TW, Bochmann S, Kötter P, Wichelhaus T, Stein T, Entian KD (2011) Entianin, a novel subtilin-like lantibiotic from Bacillus subtilis subsp. spizizenii DSM 15029T with high antimicrobial activity. Appl Environ Microbiol 77:1698–1707

  54. Garcia-Gonzalez E, Müller S, Hertlein G, Heid N, Süssmuth RD, Genersch E (2014) Biological effects of paenilamicin, a secondary metabolite antibiotic produced by the honey bee pathogenic bacterium Paenibacillus larvae. Microbiologyopen. 3:642–656

  55. Garg N, Tang W, Goto Y, Nair SK, van der Donk WA (2012) Lantibiotics from Geobacillus thermodenitrificans. Proc Natl Acad Sci U S A 109:5241–5246

  56. Gatehouse HS, Tan B, Christeller JT, Hurst MRH, Marshall SDG, Jackson TA (2009) Phenotypic changes and the fate of digestive enzymes during induction of amber disease in larvae of the New Zealand grass grub (Costelytra zealandica). J Invertebr Pathol 101:215–221

  57. Gerc AJ, Song L, Challis GL, Stanley-Wall NR, Coulthurst SJ (2012) The insect pathogen Serratia marcescens Db10 uses a hybrid nonribosomal peptide synthetase-polyketide synthase to produce the antibiotic althiomycin. PLoS One 7:e44673

  58. Gerc AJ, Stanley-Wall NR, Coulthurst SJ (2014) Role of the phosphopantetheinyl transferase enzyme, PswP, in the biosynthesis of antimicrobial secondary metabolites by Serratia marcescens Db10. Microbiol-SGM. 160:1609–1617

  59. Giri AV, Anandkumar N, Muthukumaran G, Pennathur G (2004) A novel medium for the enhanced cell growth and production of prodigiosin from Serratia marcescens isolated from soil. BMC Microbiol 4:11

  60. Glare TR, Corbett GE, Sadler AJ (1993) Association of a large plasmid with amber disease of the New Zealand grass grub, Costelytra zealandica, caused by Serratia entomophila and Serratia proteamaculans. J Invertebr Pathol 62:165–170

  61. Gokulan K, Khare S, Cerniglia C (2014) Metabolic pathways: production of secondary metabolites of bacteria. In: Batt, C.A., Tortorello, M.L. (Eds.), Encyclopedia of food microbiology, vol 2. Elsevier Ltd, Academic Press, pp. 561–569

  62. Gonzalez-Pastor JE, Hobbs EC, Losick R (2003) Cannibalism by sporulating bacteria. Science. 301:510–513

  63. Grimont PAD, Jackson TA, Ageron E, Noonan MJ (1988) Serratia entomophila sp. nov. associated with amber disease in the New Zealand grass grub Costelytra zealandica. Int J Syst Evol Microbiol 38:1–6

  64. Gross H, Loper JE (2009) Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446

  65. Gross H, Stockwell VO, Henkels MD, Nowak-Thompson B, Loper JE, Gerwick WH (2007) The genomisotopic approach: a systematic method to isolate products of orphan biosynthetic gene clusters. Chem Biol 14:53–63

  66. Guttenberger N, Blankenfeldt W, Breinbauer R (2017) Recent developments in the isolation, biological function, biosynthesis, and synthesis of phenazine natural products. Bioorg Med Chem 25:6149–6166

  67. Gutterson N, Ziegle JS, Warren GJ, Layton TL (1988) Genetic determinants for catabolite induction of antibiotic biosynthesis in Pseudomonas fluorescens HV37a. J Bacteriol 170:380–385

  68. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319

  69. Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41:117–153

  70. Harris AKP, Williamson NR, Slater H, Cox A, Abbasi S, Foulds I, Simonsen HT, Leeper FJ, Salmond GPC (2004) The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiol-SGM. 150:3547–3560

  71. 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

  72. 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 73:168–178

  73. 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 164:281–291

  74. Hellberg J, Matilla MA, Salmond GPC (2015) The broad-spectrum antibiotic, zeamine, kills the nematode worm Caenorhabditis elegans. Front Microbiol 6:137

  75. Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70:921–928

  76. Hu HB, Xu YQ, Chen F, Zhang XH, Hur BK (2005) Isolation and characterization of a new fluorescent Pseudomonas strain that produces both phenazine 1-carboxylic acid and pyoluteorin. J Microbiol Biotechnol 15:86–90

  77. Huang E, Guao Y, Yousef AE (2014) Biosynthesis of the new broad-spectrum lipopeptide antibiotic paenibacterin in Paenibacillus thiaminolyticus OSY-SE. Res Microbiol 165:243–251

  78. Hurst MRN, Becher SA, O'Callaghan M (2011) Nucleotide sequence of the Serratia entomophila plasmid pADAP and the Serratia proteamaculans pU143 plasmid virulence associated region. Plasmid. 65:32–41

  79. Ishii K, Adachi T, Imamura K, Takano S, Usui K, Suzuki K, Hamamoto H, Watanabe T, Sekimizu K (2012) Serratia marcescens induces apoptotic cell death in host immune cells via a lipopolysaccharide- and flagella-dependent mechanism. J Biol Chem 287:36582–36592

  80. Islam MT, Fukushi Y (2010) Growth inhibition and excessive branching in Aphanomyces cochlioides induced by 2,4-diacetylphloroglucinol is linked to disruption of filamentous actin cyto-skeleton in the hyphae. World J Microbiol Biotechnol 26:1163–1170

  81. Jabrane A, Sabri A, Compere P, Jacques P, Vandenberghe I, Van Beeumen J, Thonart P (2002) Characterization of serracin P, a phage-tail-like bacteriocin, and its activity against Erwinia amylovora, the fire blight pathogen. Appl Environ Microbiol 68:5704–5710

  82. Jackson TA, Pearson JF, O'Callaghan M, Mahanty HK, Willcocks MJ (1992) Pathogen to product—development of Serratia entomophila (Enterobacteriaceae) as a commercial biological agent for the New Zealand grass grub (Costelytra zealandica). In: Jackson TA, Glare TR (eds) Use of pathogens in scarab pest management. Intercept Press, Andover, pp 191–198

  83. Jackson TA, Huger AM, Glare TR (1993) Pathology of amber disease in the New-Zealand grass grub Costelytra zealandica (Coleoptera, Scarabaeidae). J Invertebr Pathol 61:123–130

  84. Jackson TA, O'Callaghan M, Glare TR (1998) Safe use of replicating bacteria in biological control. Phytoprotection. 79:50–55

  85. Jafarzade M, Yahya NA, Shayesteh F, Usup G, Ahmad A (2013) Influence of culture conditions and medium composition on the production of antibacterial compounds by marine Serratia sp WPRA3. J Microbiol 51:373–379

  86. Kadouri DE, Shanks RMQ (2013) Identification of a methicillin-resistant Staphylococcus aureus inhibitory compound isolated from Serratia marcescens. Res Microbiol 164:821–826

  87. 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

  88. Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35:323–331

  89. 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

  90. Kawulka K, Sprules T, McKay RT, Mercier P, Diaper CM, Zuber P, Vederas JC (2003) Structure of subtilosin A, an antimicrobial peptide from Bacillus subtilis with unusual posttranslational modifications linking cysteine sulfurs to alpha-carbons of phenylalanine and threonine. J Am Chem Soc 125:4726–4727

  91. 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

  92. Khare E, Arora NK (2011) Dual activity of pyocyanin from Pseudomonas aeruginosa—antibiotic against phytopathogen and signal molecule for biofilm development by rhizobia. Can J Microbiol 57:708–713

  93. Kiss A, Baliko G, Csorba A, Chuluunbaatar T, Medzihradszky KF, Alföldi L (2008) Cloning and characterization of the DNA region responsible for Megacin A-216 production in Bacillus megaterium 216. J Bacteriol 190:6448–6457

  94. Klein C, Kaletta C, Schnell N, Entian KD (1992) Analysis of genes involved in biosynthesis of the lantibiotic subtilin. Appl Environ Microbiol 58:132–142

  95. Konz D, Klens A, Schörgendorfer K, Marahiel MA (1997) The bacitracin biosynthesis operon of Bacillus licheniformis ATCC 10716: molecular characterization of three multi-modular peptide synthetases. Chem Biol 4:927–937

  96. Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borris 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

  97. Kuroda J, Fukai T, Konishi M, Ono J, Kurusu K, Nomura T (2000) LI-F antibiotics, family of antifungal cyclic depsipeptides produced by Bacillus polymyxa L-1129. Heterocycles. 53:1533–1549

  98. Le Marrec C, Hyronimus B, Bressolier 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. Appl Environ Microbiol 66:5213–5220

  99. Lee H, Kim HY (2010) Lantibiotics, class I bacteriocins from the genus Bacillus. J Microbiol Biotechnol 21:229–235

  100. 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 105:5879–5884

  101. Lee H, Churey JJ, Worobo RW (2009) Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiol Lett 299:205–213

  102. Lee X, Azevedo MD, Armstrong DJ, Banowetz GM, Reimmann C (2013) The Pseudomonas aeruginosa antimetabolite L-2-amino-4-methoxy-trans-3-butenoic acid inhibits growth of Erwinia amylovora and acts as a seed germination-arrest factor. Environ Microbiol Rep 5:83–89

  103. Levenfors JJ, Hedman R, Thaning C, Gerhardson B, Welch CJ (2004) Broad-spectrum antifungal metabolites produced by the soil bacterium Serratia plymuthica A 153. Soil Biol Biochem 36:677–685

  104. Li J, Jensen SE (2008) Nonribosomal biosynthesis of fusaricidins by Paenibacillus polymyxa PKB1 involves direct activation of a D-amino acid. Chem Biol 15:118–127

  105. Li YM, Milne JC, Madison LL, Kolter R, Walsh CT (1996) From peptide precursors to oxazole and thiazole-containing peptide antibiotics: microcin B17 synthase. Science. 274:1188–1193

  106. Li J, Beatty PK, Shah S, Jensen SE (2007) Use of PCR-targeted mutagenesis to disrupt production of fusaricidin-type antifungal antibiotics in Paenibacillus polymyxa. Appl Environ Microbiol 73:3480–3489

  107. Li XY, Mao ZC, Wang YH, Wu YX, He YQ, Long CL (2012) ESI LC-MS and MS/MS characterization of antifungal cyclic lipopeptides produced by Bacillus subtilis XF-1. J Mol Microbiol Biotechnol 22:83–93

  108. Liao R, Duan L, Lei C, Pan H, Ding Y, Zhang Q, Chen D, Shen B, Yu Y, Liu W (2009) Thiopeptide biosynthesis featuring ribosomally synthesized precursor peptides and conserved posttranslational modifications. Chem Biol 16:141–147

  109. Liu XG, Bimerew M, Ma YX, Mueller H, Ovadis M, Eberl L, Berg G, Chernin L (2007) Quorum-sensing signaling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica. FEMS Microbiol Lett 270:299–305

  110. 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 20:43–52

  111. Liu Z, Budiharjo A, Wang P, Shi H, Fang J, Borriss R, Zhang K, Huang X (2013) The highly modified microcin peptide plantazolicin is associated with nematicidal activity of Bacillus amyloliquefaciens FZB42. Appl Microbiol Biotechnol 97:10081–10090

  112. 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 134:19540–19543

  113. Lohans CT, van Belkum MJ, Cochrane SA, Huang Z, Sit CS, McMullen LM, Vederas JC (2014) Biochemical, structural, and genetic characterization of tridecaptin A1, an antagonist of Campylobacter jejuni. Chembiochem. 15:243–249

  114. Loper JE, Henkels MD, Shaffer BT, Valeriote FA, Gross H (2008) Isolation and identification of rhizoxin analogs from Pseudomonas fluorescens Pf-5 by using a genomic mining strategy. Appl Environ Microbiol 74:3085–3093

  115. Lugtenberg BJ, Chin AWTF, Bloemberg GV (2002) Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383

  116. Luo C, Liu X, Zhou X, Guo J, Truong J, Wang X, Zhou H, Chen Z (2015) Unusual biosynthesis and structure of locillomycins from Bacillus subtilis 916. Appl Environ Microbiol 81:6601–6609

  117. Maddula VS, Pierson EA, Pierson LSIII (2008) Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J Bacteriol. 190: 2759–2766

  118. Madhavachary R, Ramachary DB (2014) High-yielding total synthesis of sexually deceptive chiloglottones and antimicrobial dialkylresorcinols through an organocatalytic reductive coupling reaction. Eur J Org Chem:7317–7323

  119. Mahlen SD (2011) Serratia infections: from military experiments to current practice. Clin Microbiol Rev 24:755–791

  120. Mai AGM (2018) Serratia a novel source of secondary metabolites. Adv Biotech & Micro 11:555814

  121. Marchand PA, Weller DM, Bonsall RF (2000) Convenient synthesis of 2,4-diacetylphloroglucinol, a natural antibiotic involved in the control of take-all disease of wheat. J Agric Food Chem 48:1882–1887

  122. Masschelein J, Mattheus W, Gao LJ, Moons P, Van Houdt R, Uytterhoeven B, Lamberigts C, Lescrinier E, Rozenski J, Herdewijn P, Aertsen A, Michiels C, Lavigne R (2013) A PKS/NRPS/FAS hybrid gene cluster from Serratia plymuthica RVH1 encoding the biosynthesis of three broad spectrum, zeamine-related antibiotics. PLoS One. 8

  123. Mavrodi OV, McSpadden Gardener BB, Mavrodi DV, Bonsall RF, Weller DM, Thomashow LS (2001) Genetic diversity of phlD from 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species. Phytopathol. 91:35–43

  124. Mavrodi DV, Blankenfeldt W, Thomashow LS, Mentel M (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445

  125. Mavrodi DV, Parejko JA, Mavrodi OV, Kwak YS, Weller DM, Blankenfeldt W, Thomashow LS (2013) Recent insights into the diversity, frequency and ecological roles of phenazines in fluorescent Pseudomonas spp. Environ Microbiol 15:675–686

  126. 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 103:17243–17248

  127. McPhail KL, Armstrong DJ, Azevedo MD, Banowetz GM, Mills DI (2010) 4-Formyl amino oxyvinylglycine, an herbicidal germination-arrest factor from Pseudomonas rhizosphere bacteria. J Nat Prod 73:1853–1857

  128. McSpadden Gardener BB, Fravel DR (2002) Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Health Progress. https://doi.org/10.1094/PHP-2002-0510-01-RV

  129. Medema MH, Kottmann R, Yilmaz P, Cummings M, Biggins JB, Blin K, de Bruijn I, Chooi YH, Claesen J, Coates RC, Cruz-Morales P, Duddela S, Düsterhus S, Edwards DJ, Fewer DP, Garg N, Geiger C, Gomez-Escribano JP, Greule A, Hadjithomas M, Haines AS, Helfrich EJ, Hillwig ML, Ishida K, Jones AC, Jones CS, Jungmann K, Kegler C, Kim HU, Kötter P, Krug D, Masschelein J, Melnik AV, Mantovani SM, Monroe EA, Moore M, Moss N, Nützmann HW, Pan G, Pati A, Petras D, Reen FJ, Rosconi F, Rui Z, Tian Z, Tobias NJ, Tsunematsu Y, Wiemann P, Wyckoff E, Yan X, Yim G, Yu F, Xie Y, Aigle B, Apel AK, Balibar CJ, Balskus EP, Barona-Gómez F, Bechthold A, Bode HB, Borriss R, Brady SF, Brakhage AA, Caffrey P, Cheng YQ, Clardy J, Cox RJ, De Mot R, Donadio S, Donia MS, van der Donk WA, Dorrestein PC, Doyle S, Driessen AJ, Ehling-Schulz M, Entian KD, Fischbach MA, Gerwick L, Gerwick WH, Gross H, Gust B, Hertweck C, Höfte M, Jensen SE, Ju J, Katz L, Kaysser L, Klassen JL, Keller NP, Kormanec J, Kuipers OP, Kuzuyama T, Kyrpides NC, Kwon HJ, Lautru S, Lavigne R, Lee CY, Linquan B, Liu X, Liu W, Luzhetskyy A, Mahmud T, Mast Y, Méndez C, Metsä-Ketelä M, Micklefield J, Mitchell DA, Moore BS, Moreira LM, Müller R, Neilan BA, Nett M, Nielsen J, O'Gara F, Oikawa H, Osbourn A, Osburne MS, Ostash B, Payne SM, Pernodet JL, Petricek M, Piel J, Ploux O, Raaijmakers JM, Salas JA, Schmitt EK, Scott B, Seipke RF, Shen B, Sherman DH, Sivonen K, Smanski MJ, Sosio M, Stegmann E, Süssmuth RD, Tahlan K, Thomas CM, Tang Y, Truman AW, Viaud M, Walton JD, Walsh CT, Weber T, van Wezel GP, Wilkinson B, Willey JM, Wohlleben W, Wright GD, Ziemert N, Zhang C, Zotchev SB, Breitling R, Takano E, Glöckner FO (2015) Minimum information about a biosynthetic gene cluster. Nat Chem Biol 11:625–631

  130. Mezaache-Aichour S, Guechi A, Nicklin J, Drider D, Prevost H (2012) Isolation, identification and antimicrobial activity of pseudomonads isolated from the rhizosphere of potatoes growing in Algeria. J Plant Pathol 94:89–98

  131. Mishra J, Arora NK (2018) Secondary metabolites of fluorescent pseudomonads in biocontrol of phytopathogens for sustainable agriculture. Appl Soil Ecol 125:35–45

  132. Moldenhauer J, Chen XH, Borriss R, Piel J (2007) Biosynthesis of the antibiotic bacillaene produced by a giant polyketide synthase complex of the trans-AT family. Angew Chem Int Ed Eng 46:8195–8197

  133. Moldenhauer J, Götz DC, 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 Eng 49:4065–4067

  134. Molohon KJ, Melby JO, Lee J, Evans BS, Dunbar KL, Bumpus SB, Kelleher NL, Mitchell DA (2011) Structure determination and interception of biosynthetic intermediates for the plantazolicin class of highly discriminating antibiotics. ACS Chem Biol 6:1307–1313

  135. 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

  136. Nielsen TH, Christophersen C, Anthoni U, Sorensen J (1999) Viscosinamide, a new cyclic depsipeptide with surfactant and antifungal properties produced by Pseudomonas fluorescens DR54. J Appl Microbiol 87:80–90

  137. Nielsen TH, Thrane C, Christophersen C, Anthoni U, Sørensen J (2000) Structure, production characteristics and fungal antagonism of tensin—a new antifungal cyclic lipopeptide from Pseudomonas fluorescens strain 96.578. J Appl Microbiol 89:992–1001

  138. 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

  139. 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

  140. Niu HT, Liu BS, Li YT, Guo HF (2016) Identification of a bacterium isolated from the diseased brown planthopper and determination of its insecticidal activity. Biocontrol Sci Tech 26:217–226

  141. O’Callaghan M, Garnham ML, Nelson TL, Baird D, Jackson TA (1996) The pathogenicity of Serratia strains to Lucilia sericata (Diptera: Calliphoridae). J Invertebr Pathol 68:22–27

  142. Oscariz JC, Pisabarro AG (2000) Characterization and mechanism of action of cerein 7, a bacteriocin produced by Bacillus cereus Bc7. J Appl Microbiol 89:361–369

  143. 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

  144. Paik SH, Chakicherla A, Hansen JN (1998) 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 273:23134–23142

  145. Patil CD, Patil SV, Salunke BK, Salunkhe RB (2011) Prodigiosin produced by Serratia marcescens NMCC46 as a mosquito larvicidal agent against Aedes aegypti and Anopheles stephensi. Parasitol Res 109:1179–1187

  146. Peipoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–563

  147. Perneel M, D’hondt L, De Maeyer K, Adiobo A, Rabaey K, Höfte M (2008) Phenazines and biosurfactants interact in the biological control of soilborne diseases caused by Pythium spp. Environ Microbiol 10:778–788

  148. Petersen LM, Tisa LS (2013) Friend or foe? A review of the mechanisms that drive Serratia towards diverse lifestyles. Can J Microbiol 59:627–640

  149. Phelan RW, Barret M, Cotter PD, O’Connor PM, Chen R, Morissey JP, Dobson AD, O’Gara F, Barbosa TM (2013) Subtilomycin: a new lantibiotic from Bacillus subtilis strain MMA7 isolated from the marine sponge Haliclona simulans. Mar Drugs 11:1878–1898

  150. Pineda-Castellanos ML, Rodriguez-Segura Z, Villalobos FJ, Hernandez L, Lina L, Nunez-Valdez ME (2015) Pathogenicity of isolates of Serratia marcescens towards larvae of the scarab Phyllophaga Blanchardi (Coleoptera). Pathogens. 4:210–228

  151. Price-Whelan A, Dietrich LE, Newman DK (2006) Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78

  152. Qian CD, Liu TZ, Zhou SL, Ding R, Zhao WP, Li O, Wu XC (2012) Identification and functional analysis of gene cluster involvement in biosynthesis of the cyclic lipopeptide antibiotic pelgipeptin produced by Paenibacillus elgii. BMC Microbiol 12:197

  153. Rahul S, Chandrashekhar P, Hemant B, Chandrakant N, Laxmikant S, Satish P (2014) Nematicidal activity of microbial pigment from Serratia marcescens. Nat Prod Res 28:1399–1404

  154. Ramette A, Frapolli M, Défago G, Moënne-Loccoz Y (2003) Phylogeny of HCN synthase-encoding hcnBC genes in biocontrol fluorescent pseudomonads and its relationship with host plant species and HCN synthesis ability. Mol Plant-Microbe Interact 16:525–535

  155. Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941

  156. Rea MC, Sit CS, Clayton E, O’Connor M, 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. Proc Natl Acad Sci U S A 107:9352–9357

  157. Rezzonico F, Zala M, Keel C, Duffy B, Moënne-Loccoz Y, Défago G (2007) Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2,4-diacetylphloroglucinol really synonymous with higher plant protection? New Phytol 173:861–872

  158. Rodriguez-Segura Z, Chen J, Villalobos FJ, Gill S, Nunez-Valdez EM (2012) The lipopolysaccharide biosynthesis core of the Mexican pathogenic strain Serratia entomophila is associated with toxicity to larvae of Phyllophaga blanchardi. J Invertebr Pathol 110:24–32

  159. Romero-Tabarez M, Jansen B, Sylla M, Luensdorf H, Häussler S, Santosa DA, Timmis KN, Molinari G (2006) 7-O-Malonyl macrolactin A, a new macrolactin antibiotiic from Bacillus subtilis—active against methicillin-resistent Staphylococcus aureus, vancomycin-resistent enterococci and a small-colony variant of Burkholderia cepacia. Antimicrob Agents Chemother 50:1701–1709

  160. Sanchez LA, Hedstrom M, Delgado MA, Delgado OD (2010) Production, purification and characterization of serraticin A, a novel cold-active antimicrobial produced by Serratia proteamaculans 136. J Appl Microbiol 109:936–945

  161. Sansinenea E (2012) Bacillus thuringiensis biotechnology. Springer, Netherlands

  162. Sansinenea E (2019a) Applications and patents of Bacillus spp. in agriculture. In: Singh HB et al (eds) Intellectual property issues in microbiology. Springer Nature, pp 133–146

  163. Sansinenea E (2019b) Bacillus spp.: as plant growth-promoting bacteria. In: Singh HB, Keswani C, Reddy MS, Sansinenea E, Garcia-Estrada C (eds) Secondary metabolites of plant growth promoting rhizomicroorgamisms. Springer, Singapore, p 225

  164. Sansinenea E, Ortiz A (2011) Secondary metabolites of soil Bacillus spp. Biotechnol Lett 33:1523–1538

  165. Sansinenea E, Ortiz A (2012) Zwittermicin A: a promising aminopolyol antibiotic from biocontrol bacteria. Curr Org Chem 16:978–987

  166. Sansinenea E, Ortiz A (2015) Melanin: a photoprotection for Bacillus thuringiensis based biopesticides. Biotechnol Lett 37:483–490

  167. Sansinenea E, Salazar F, Ramírez M, Ortiz A (2015) A UV tolerant wild-type strain of Bacillus thuringiensis with antagonistic effect producing melanin. Jundish J Microbiol 8:e20910

  168. 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 70:1417–1423

  169. Schnider-Keel U, Seematter A, Maurhofer M, Blumer C, Duffy B, Gigot-Bonnefoy C, Reimmann C, Notz R, Défago G, Haas D, Keel C (2000) Autoinduction of 2,4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J Bacteriol 182:1215–1225

  170. Scholz R, Molohon KJ, Nachtigall J, Vater J, Markley AL, Süssmuth RD, Mitchell DA, Borriss R (2011) Plantazolicin, a novel microcin B17/streptolysin S-like natural product from Bacillus amyloliquefaciens FZB42. J Bacteriol 193:215–224

  171. 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 196:1842–1852

  172. Schöner TA, Kresovic D, Bode HB (2015) Biosynthesis and function of bacterial dialkyl resorcinol compounds. Appl Microbiol Biotechnol 99:8323–8328

  173. Shaheen M, Li J, Ross AC, Vederas JC, Jensen SE (2011) Paenibacillus polymyxa PKB1 produces variants of polymyxin B-type antibiotics. Chem Biol 18:1640–1648

  174. Shahid I, Rizwan M, Baig DN, Salem RS, Mali KA, Mehnaz S (2017) Secondary metabolites production and plant growth promotion by Pseudomonas chlororaphis and P. aurantiaca strains isolated from cactus, cotton, and para grass. J Microbiol Biotechnol 27:480–491

  175. Shenkarev ZO, Finkina EI, Nurmukhamedova EK, Balandin SV, Mineev KS, Nadezhdin KD, Yakimenko ZA, Tagaev AA, Temirov YV, Arseniev AS, Ovchinnikova TV (2010) Isolation, structure elucidation, and synergistic antibacterial activity of a novel two-component lantibiotic lichenicidin from Bacillus licheniformis VK21. Biochemistry. 49:6462–6472

  176. Singh BP, Rateb ME, Rodriguez-Couto S, Teixeira de Moraes Polizeli ML, Li W-J (2019) Editorial: microbial secondary metabolites: recent developments and technological challenges. Front Microbiol 10:914

  177. Slater H, Crow M, Everson L, Salmond GPC (2003) Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol 47:303–320

  178. Someya N, Nakajima M, Watanabe K, Hibi T, Akutsu K (2005) Potential of Serratia marcescens strain B2 for biological control of rice sheath blight. Biocontrol Sci Tech 15:105–109

  179. Sood S, Steinmetz H, Beims H, Mohr KI, Stadler M, Djukic M, von der Ohe W, Steinert M, Daniel R, Müller R (2014) Paenilarvins: Iturin family lipopeptides from the honey bee pathogen Paenibacillus larvae. Chembiochem. 15:1947–1955

  180. Spago FR, Ishii Mauro CS, Oliveira AG, Beranger JPO, Cely MVT, Stanganelli MM, Simionato AS, San Martin JAB, Andrade CGTJ, Mello JCP, Andrade G (2014) Pseudomonas aeruginosa produces secondary metabolites that have biological activity against plant pathogenic Xanthomonas species. Crop Prot 62:46–54

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

  182. 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 184:1703–1711

  183. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75:748–757

  184. Taira E, Mon H, Lee JM, Kusakabe T, Yasunaga-Aoki C, Iiyama K (2016) Virulence of lipopolysaccharide-deficient mutants of Serratia liquefaciens toward the silkworm, Bombyx mori. J Insect Biotechnol Sericology 5:7–14

  185. Tambadou F, Caradec T, Gagez AL, Bonnet A, Sopena V, Bridiau N, Thiery V, Didelot S, Barthelemy C, Chevrot R (2015) Characterization of the colistin (polymyxin E1 and E2) biosynthetic gene cluster. Arch Microbiol 197:521–532

  186. Tan B, Jackson TA, Hurst MRH (2006) Virulence of Serratia strains against Costelytra zealandica. Appl Environ Microbiol 72:6417–6418

  187. Tang XJ, Thibault P, Boyd RK (1992) Characterisation of the tyrocidine and gramicidin fractions of the tyrothricin complex from Bacillus brevis using liquid chromatography and mass spectrometry. Int J Mass Spectrom Ion Process 122:153–179

  188. Tao K, Long Z, Liu K, Tao Y, Liu S (2006) Purification and properties of a novel insecticidal protein from the locust pathogen Serratia marcescens HR-3. Curr Microbiol 52:45–49

  189. Thane C, Nielsen TH, Neiendam M, Sørensen J, Olsson S (2000) Viscosinamid-producing Pseudomonas fluorescens DR54 exerts a biocontrol effect on Pythium ultimum in sugar beet rhizosphere. FEMS Microbiol Ecol 33:139–146

  190. Theodore CM, Stamps BW, King JB, Price LS, Powell DR, Stevenson BS, Cichewicz RH (2014) Genomic and metabolomic insights into the natural product biosynthetic diversity of a feral-hog-associated Brevibacillus laterosporus strain. PLoS One 9:e90124

  191. Thies S, Santiago-Schübel B, Kovačić F, Rosenau F, Hausmann R, Jaeger KE (2014) Heterologous production of the lipopeptide biosurfactant serrawettin W1 in Escherichia coli. J Biotechnol 181:27–30

  192. Tofazzal IM, von Tiedemann A (2011) 2,4-Diacetylphloroglucinol suppresses zoosporogenesis and impairs motility of Peronosporomycete zoospores. World J Microbiol Biotechnol 27:2071–2079

  193. Tsuge K, Akiyama T, Shoda M (2001) Cloning, sequencing, and characterization of the iturin A operon. J Bacteriol 183:6265–6273

  194. van Belkum MJ, Martin-Visscher LA, Vederas JC (2011) Structure and genetics of circular bacteriocins. Trends Microbiol 19:411–418

  195. Van Pée KH, Ligon JM (2000) Biosynthesis of pyrrolnitrin and other phenylpyrrole derivatives by bacteria. Nat Prod Rep 17:157–164

  196. Veit B, Herzberg C, Steckel S, Feesche J, Maurer KH, Ehrenreich P, Bäumer S, Henne A, Liesegang H, Merkl R, Ehrenreich A, Gottschalk G (2004) The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. J Mol Microbiol Biotechnol 7:204–211

  197. Velusamy P, Immanuel JE, Gnanamanickam SS, Thomashow L (2006) Biological control of rice bacterial leaf blight by plant-associated bacteria producing 2,4 diacetylphloroglucinol. Can J Microbiol 52:56–65

  198. Visnovsky GA, Smalley DJ, O'Callaghan M, Jackson TA (2008) Influence of culture medium composition, dissolved oxygen concentration and harvesting time on the production of Serratia entomophila, a microbial control agent of the New Zealand grass grub. Biocontrol Sci Tech 18:87–100

  199. Wang J, Zhang L, Teng K, Sun S, Sun Z, Zhong J (2014) Cerecidins, novel lantibiotics from Bacillus cereus with potent antimicrobial activity. Appl Environ Microbiol 80:2633–2643

  200. Wieland Brown LC, Acker MG, Clardy J, Walsh CT, Fischbach MA (2009) Thirteen posttranslational modifications convert a 14-residue peptide into the antibiotic thiocillin. Proc Natl Acad Sci U S A 106:2549–2553

  201. Wilf NM, Reid AJ, Ramsay JP, Williamson NR, Croucher NJ, Gatto L, Hester SS, Goulding D, Barquist L, Lilley KS, Kingsley RA, Dougan G, Salmond GPC (2013) RNA-seq reveals the RNA binding proteins, Hfq and RsmA, play various roles in virulence, antibiotic production and genomic flux in Serratia sp ATCC 39006. BMC Genomics 14

  202. Williamson NR, Fineran PC, Leeper FJ, Salmond GPC (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4:887–899

  203. Williamson NR, Fineran PC, Ogawa W, Woodley LR, Salmond GPC (2008) Integrated regulation involving quorum sensing, a two-component system, a GGDEF/EAL domain protein and a post-transcriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia. Environ Microbiol 10:1202–1217

  204. Wu DQ, Ye J, Ou HY, Wei X, Huang X, He YW, Xu Y (2011a) Genomic analysis and temperature-dependent transcriptome profiles of the rhizosphere originating strain Pseudomonas aeruginosa M18. BMC Genomics 12:438

  205. Wu XC, Qian CD, Fang HH, Wen YP, Zhou JY, Zhan ZJ, Ding R, Li O, Gao H (2011b) Paenimacrolidin, a novel macrolide antibiotic from Paenibacillus sp. F6-B70 active against methicillin-resistant Staphylococcus aureus. Microb Biotechnol 4:491–502

  206. Wu B, Oesker V, Wiese J, Schmaljohann R, Imhoff JF (2014) Two new antibiotic pyridones produced by a marine fungus, Trichoderma sp. strain MF 106. Mar Drugs 12:1208–1219

  207. 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

  208. 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 16:4889–4892

  209. 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

  210. Zhou Q, Su J, Jiang H, Huang X, Xu Y (2010) Optimization of phenazine-1-carboxylic acid production by a gacA/qscR-inactivated Pseudomonas sp. M18GQ harboring pME6032Phz using response surface methodology. Appl Microbiol Biotechnol 86:1761–1773

  211. Živković S, Stojanović S, Ivanović Ž, Gavrilović V, Popović T, Balaž J (2010) Screening of antagonistic activity of microorganisms against Colletotrichum acutatum and Colletotrichum gloeosporioides. Arch Biol Sci Belgrade 62:611–623

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Keswani, C., Singh, H.B., García-Estrada, C. et al. Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides. Appl Microbiol Biotechnol 104, 1013–1034 (2020) doi:10.1007/s00253-019-10300-8

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Keywords

  • Antimicrobials
  • Secondary metabolites
  • Agriculture
  • Pesticides