Plantazolicin, a Novel Microcin B17/streptolysin S-like Natural Product from Bacillus Amyloliquefaciens FZB42

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2010 Oct 26

PMID 20971906

Citations 83

Authors

Romy Scholz

Katie J Molohon

Jonny Nachtigall

Joachim Vater

Andrew L Markley

Roderich D Sussmuth

Douglas A Mitchell

Rainer Borriss

Affiliations

Soon will be listed here.

Abstract

Here we report on a novel thiazole/oxazole-modified microcin (TOMM) from Bacillus amyloliquefaciens FZB42, a Gram-positive soil bacterium. This organism is well known for stimulating plant growth and biosynthesizing complex small molecules that suppress the growth of bacterial and fungal plant pathogens. Like microcin B17 and streptolysin S, the TOMM from B. amyloliquefaciens FZB42 undergoes extensive posttranslational modification to become a bioactive natural product. Our data show that the modified peptide bears a molecular mass of 1,335 Da and displays antibacterial activity toward closely related Gram-positive bacteria. A cluster of 12 genes that covers ∼10 kb is essential for the production, modification, export, and self-immunity of this natural product. We have named this compound plantazolicin (PZN), based on the association of several producing organisms with plants and the incorporation of azole heterocycles, which derive from Cys, Ser, and Thr residues of the precursor peptide.

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References

Wieland Brown L, Acker M, Clardy J, Walsh C, Fischbach M . Thirteen posttranslational modifications convert a 14-residue peptide into the antibiotic thiocillin. Proc Natl Acad Sci U S A. 2009; 106(8):2549-53. PMC: 2650375. DOI: 10.1073/pnas.0900008106. View

Choudhary D, Johri B . Interactions of Bacillus spp. and plants--with special reference to induced systemic resistance (ISR). Microbiol Res. 2008; 164(5):493-513. DOI: 10.1016/j.micres.2008.08.007. View

Vetting M, Hegde S, Fajardo J, Fiser A, Roderick S, Takiff H . Pentapeptide repeat proteins. Biochemistry. 2006; 45(1):1-10. PMC: 2566302. DOI: 10.1021/bi052130w. View

Chen X, Koumoutsi A, Scholz R, Schneider K, Vater J, Sussmuth R . Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol. 2008; 140(1-2):27-37. DOI: 10.1016/j.jbiotec.2008.10.011. View

Haft D, Basu M, Mitchell D . Expansion of ribosomally produced natural products: a nitrile hydratase- and Nif11-related precursor family. BMC Biol. 2010; 8:70. PMC: 2887384. DOI: 10.1186/1741-7007-8-70. View

Koumoutsi A, Chen X, Vater J, Borriss R . DegU and YczE positively regulate the synthesis of bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl Environ Microbiol. 2007; 73(21):6953-64. PMC: 2074971. DOI: 10.1128/AEM.00565-07. View

HARDONK M, VAN DUIJN . THE MECHANISM OF THE SCHIFF REACTION AS STUDIED WITH HISTOCHEMICAL MODEL SYSTEMS. J Histochem Cytochem. 1964; 12:748-51. DOI: 10.1177/12.10.748. View

Koumoutsi A, Chen X, Henne A, Liesegang H, Hitzeroth G, Franke P . Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol. 2004; 186(4):1084-96. PMC: 344220. DOI: 10.1128/JB.186.4.1084-1096.2004. View

Pei J, Grishin N . Type II CAAX prenyl endopeptidases belong to a novel superfamily of putative membrane-bound metalloproteases. Trends Biochem Sci. 2001; 26(5):275-7. DOI: 10.1016/s0968-0004(01)01813-8. View

10.

Morris R, Leeds J, Naegeli H, Oberer L, Memmert K, Weber E . Ribosomally synthesized thiopeptide antibiotics targeting elongation factor Tu. J Am Chem Soc. 2009; 131(16):5946-55. DOI: 10.1021/ja900488a. View

11.

Lee S, Mitchell D, Markley A, Hensler M, Gonzalez D, Wohlrab A . Discovery of a widely distributed toxin biosynthetic gene cluster. Proc Natl Acad Sci U S A. 2008; 105(15):5879-84. PMC: 2311365. DOI: 10.1073/pnas.0801338105. View

12.

Cotter P, Draper L, Lawton E, Daly K, Groeger D, Casey P . Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog. 2008; 4(9):e1000144. PMC: 2522273. DOI: 10.1371/journal.ppat.1000144. View

13.

Rodriguez-Martinez J, Briales A, Velasco C, Conejo M, Martinez-Martinez L, Pascual A . Mutational analysis of quinolone resistance in the plasmid-encoded pentapeptide repeat proteins QnrA, QnrB and QnrS. J Antimicrob Chemother. 2009; 63(6):1128-34. DOI: 10.1093/jac/dkp111. View

14.

Dirix G, Monsieurs P, Marchal K, Vanderleyden J, Michiels J . Screening genomes of Gram-positive bacteria for double-glycine-motif-containing peptides. Microbiology (Reading). 2004; 150(Pt 5):1121-1126. DOI: 10.1099/mic.0.27040-0. View

15.

Oman T, van der Donk W . Insights into the mode of action of the two-peptide lantibiotic haloduracin. ACS Chem Biol. 2009; 4(10):865-74. PMC: 2812937. DOI: 10.1021/cb900194x. View

16.

Butcher B, Helmann J . Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol Microbiol. 2006; 60(3):765-82. DOI: 10.1111/j.1365-2958.2006.05131.x. View

17.

Horton R, Cai Z, Ho S, Pease L . Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques. 1990; 8(5):528-35. View

18.

Chen X, Koumoutsi A, Scholz R, Borriss R . More than anticipated - production of antibiotics and other secondary metabolites by Bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol. 2008; 16(1-2):14-24. DOI: 10.1159/000142891. View

19.

Datta V, Myskowski S, Kwinn L, Chiem D, Varki N, Kansal R . Mutational analysis of the group A streptococcal operon encoding streptolysin S and its virulence role in invasive infection. Mol Microbiol. 2005; 56(3):681-95. DOI: 10.1111/j.1365-2958.2005.04583.x. View

20.

Borriss R, Chen X, Rueckert C, Blom J, Becker A, Baumgarth B . Relationship of Bacillus amyloliquefaciens clades associated with strains DSM 7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete.... Int J Syst Evol Microbiol. 2010; 61(Pt 8):1786-1801. DOI: 10.1099/ijs.0.023267-0. View