The highly modified microcin peptide plantazolicin is associated with nematicidal activity of Bacillus amyloliquefaciens FZB42

Applied Microbiology and Biotechnology

Volumn 97, Issue 23, 2013, Pages 10081-10090

  Liu, Zhongzhong ^a,b   Budiharjo, Anto ^c   Wang, Pengfei ^a   Shi, Hui ^a   Fang, Juan ^a   Borriss, Rainer ^d,e   Zhang, Keqin ^a   Huang, Xiaowei ^a  

^a YUNNAN UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c DIPONEGORO UNIVERSITY   (Indonesia)

^d HUMBOLDT UNIVERSITY   (Germany)

^e ABiTEP   (Germany)

Author keywords

Bacillus amyloliquefaciens FZB42; ESI TOF MS; Himar1 transposon library; Nematicidal activity; Plantazolicin; RBAM 007470 gene

Indexed keywords

ANTAGONISTIC EFFECTS; BACILLUS AMYLOLIQUEFACIENS; ESI-TOF-MS; MARINER TRANSPOSON; NEMATICIDAL ACTIVITY; PATHOGENIC ORGANISMS; PLANTAZOLICIN; TIME OF FLIGHT MASS SPECTROMETRY;

BACTERIOLOGY; BIOASSAY; BIOCHEMISTRY; ELECTROSPRAY IONIZATION; INDUCTIVELY COUPLED PLASMA;

GENES;

ANTINEMATODAL AGENT; PLANTAZOLICIN; UNCLASSIFIED DRUG;

BIOASSAY; EXPERIMENTAL STUDY; GROWTH RATE; MICROBIAL ACTIVITY; MUTAGENICITY; NEMATODE; PEPTIDE; PLANT COMMUNITY; POLYMERASE CHAIN REACTION;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACTERIAL GENETICS; BACTERIAL STRAIN; BIOASSAY; CONTROLLED STUDY; DRUG SYNTHESIS; GENE DELETION; MOLECULAR LIBRARY; MOLECULAR WEIGHT; NONHUMAN; POLYMERASE CHAIN REACTION; TIME OF FLIGHT MASS SPECTROMETRY; TRANSPOSON;

ANIMALS; ANTINEMATODAL AGENTS; BACILLUS; BACTERIAL PROTEINS; BACTERIOCINS; BASE SEQUENCE; MOLECULAR SEQUENCE DATA; NEMATODA; OLIGOPEPTIDES;

EID: 84888151645     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5247-5     Document Type: Article

References (44)

1. Åhman J (2000) Extracellular serine proteases as virulence factors in nematophagous fungi: molecular characterization and functional analysis of the PII protease in Arthrobotrys oligospora. PhD thesis, University of Lund, Lund, Sweden
2. Arraez-Roman D, Fu SQ, Sawalha SMS, Segura-Carretero A, Fernández-Gutiérrez A (2010) HPLC/CE-ESI-TOF-MS methods for the characterization of polyphenols in almond-skin extracts. Electrophoresis 31:2289-2296
3. Atibalentja N, Noel GR, Domier LL (2000) Phylogenetic position of the North American isolates of Pasteuria that parasitizes the soybean cyst nematodes, Heterodera glycines, as inferred from 16S rDNA sequence analysis. Int J Syst Evol Microbiol 50:605-613
4. Bravo A, Sarabia S, Lopez L, Ontiveros H, Abarca C, Ortiz A, Ortiz M, Lina L, Villalobos FJ, Peña G, Nuñez-Valdez ME, Soberón M, Quintero R (1998) Characterization of cry genes in a Mexican Bacillus thuringiensis strain collection. Appl Environ Microbiol 64:4965-4972
5. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94
6. Burkett-Cadena M, Kokalis-Burelle N, Lawrence KS, van Santen E, Kloepper JW (2008) Suppressiveness of root-knot nematodes mediated by rhizobacteria. Biol Control 47:55-59
7. Cameron DE, Urbach JM, Mekalanos JJ (2008) A defined transposon mutant library and its use in identifying motility genes in Vibrio cholera. Proc Natl Acad Sci U S A 105:8736-8741
8. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Süssmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007-1014
9. Crickmore N (2005) Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol 13:347-350
10. Datta V, Myskowski SM, Kwinn LA, Chiem DN, Varki N, Kansal RG, Kotb M, Nizet V (2005) Mutational analysis of the group A streptococcal operon encoding streptolysin S and its virulence role in invasive infection. Mol Microbiol 56:681-695
11. Dietel K, Beator B, Budiharjo A, Fan B, Borriss R (2013) Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol J 29:59-66
12. Duncon LW (1991) Current options for nematode management. Annu Rev Phytopathol 29:469-490
13. Earl AM, Eppinger M, Fricke WF, Rosovitz MJ, Rasko DA, Daugherty S, Losick R, Kolter R, Ravel J (2012) Whole-genome sequences of Bacillus subtilis and close relatives. J Bacteriol 194:2378-2379
14. Ebert D, Rainey P, Embley TM, Scholz D (1996) Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ranosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna Straus. Philos Trans R Soc Lond B 351:1689-1701
15. Fischer C, Geourjon C, Bourson C, Deutscher J (1996) Cloning and characterization of the Bacillus subtilis prkA gene encoding a novel serine protein kinase. Gene 168:55-60
16. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, Murray BE, Calderwood SB, Ausubel FM (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 98:10892-10897
17. Garvis S, Munder A, Ball G, Bentzmann SD, Wiehlmann L, Ewbank JJ, Tümmler B, Filloux A (2009) Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. PLoS Pathog 5(8):1-13
18. Haft DH, Basu MK, Mitchell DA (2010) Expansion of ribosomally produced natural products: a nitrile hydratase- and Nif11-related precursor family. BMC Biol 8:70
19. Huang XW, Tian BY, Niu QH, Yang JK, Zhang LM, Zhang KQ (2005) An extracellular protease from Brevibacillus laterosporus G4 without parasporal crystal can serve as a pathogenic factor in infection of nematodes. Res Microbiol 156:719-727
20. Idris ESE, 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
21. Kalyon B, Helaly SE, Scholz R, Nachtigall J, Vater J, Borriss R, Süssmuth RD (2011) Plantazolicin A and B: structure elucidation of ribosomally synthesized thiazole/oxazole peptides from Bacillus amyloliquefaciens FZB42. Org Lett 13:2996-2999
22. Kotze AC, O'Grady J, Gough JM, Pearson R, Bagnall NH, Kemp DH, Akhurst RJ (2005) Toxicity of Bacillus thuringiensis to parasitic and free-living life stages of nematodes parasites of livestock. Int J Parasitol 35:1013-1022
23. Kunst F, Rapoport G (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177:2403-2407
24. Kurz CL, Ewbank JJ (2000) Caenorhabditis elegans for the study of host-pathogen interactions. Trends Microbiol 8:142-144
25. Kurz CL, Chauvet S, Andres E, Aurouze M, Vallet I, Michel GPF, Uh M, Celli J, Filloux A, Bentzmann SD, Steinmetz I, Hoffmann JA, Finlay BB, Gorvel JP, Ferrandon D, Ewbank JJ (2003) Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J 22:1451-1460
26. Le Breton YL, Mohapatra NP, Haldenwang WG (2006) In vivo random mutagenesis of Bacillus subtilis by sse of TnYLB-1, a mariner-based transposon. Appl Environ Microbiol 72:327-333
27. Lewis JA, Fleming JT (1995) Basic culture methods. In: Epstein HF and Shakes DC (eds) Caenorhabditis elegans: modern biological analysis of an organism. Academic, San Diego, CA, pp 3-29
28. 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
29. Marroquin LD, Elyassnia D, Griffitts JS, Feitelson JS, Aroian RV (2000) Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics 155:1693-1699
30. Milne JC, Roy RS, Eliot AC, Kelleher NL, Wokhlu A, Nickels B, Walsh CT (1999) Cofactor requirements and reconstitution of microcin B17 synthetase: a multienzyme complex that catalyzes the formation of oxazoles and thiazoles in the antibiotic microcin B17. Biochemistry 38:4768-4781
31. Molohon K, 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 16:1307-1313
32. Niu QH, Huang XW, Zhang L, Yang JK, Zhang KQ (2006) A neutral protease from Bacillus nematocida, another potential virulence factor in the infection against nematodes. Arch Microbiol 185:439-448
33. Niu QH, Huang XW, Zhang L, Lian LH, Li YX, Li J, Yang JK, Zhang KQ (2007) Functional identification of the gene bace16 from nematophagous bacterium Bacillus nematocida. Appl Microbiol Biotechnol 75:141-148
34. O'Quinn AL, Wiegand EM, Jeddeloh JA (2001) Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell Microbiol 3:381-393
35. Qin X, Singh KV, Weinstock GM, Murray BE (2000) Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect Immun 68:2579-2586
36. Schneider SM, Rosskopf EN, Leesch JG, Chellemi DO, Bull CT, Mazzola M (2003) Research on alternatives to methyl bromide: pre-plant and post-harvest. Pest Manag Sci 59:814-826
37. 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
38. Shin-ya K, Wierzba K, Matsuo K, Ohtani T, Yamada Y, Furihata K, Hayakawa Y, Seto H (2001) Telomestatin, a novel telomerase inhibitor from Streptomyces anulatus. J Am Chem Soc 131:1262-1263
39. Sifri CD, Mylonakis E, Singh KV, Qin X, Garsin DA, Murray BE, Ausubel FM, Calderwood SB (2002) Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70:5647-5650
40. Tian BY, Yang JK, Zhang KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol Ecol 61:197-213
41. Tikhonov VE, Lopez-Llorca LV, Salinas J, Jansson HB (2002) Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V. suchlasporium. Fungal Genet Biol 35:67-78
42. Valverde A, Aguilera A, Ferrer CA, Camacho F, Cammarano A (2010) Analysis of forchlorfenuron in vegetables by LC/TOF-MS after extraction with the buffered QuEChERS method. J Agric Food Chem 58:2818-2823
43. Wei JZ, Hale K, Carta L, Platzer E, Wong C, Fang SC, Aroian RV (2003) Bacillus thuringiensis crystal proteins that target nematodes. Proc Natl Acad Sci U S A 100:2760-2765
44. Xia YF, Xie SS, Ma X, Wu HJ, Wang X, Gao XW (2011) The purL gene of Bacillus subtilus is associated with nematicidal activity. FEMS Microbiol Lett 322:99-107