Biosynthetic Mechanism for Sunscreens of the Biocontrol Agent Lysobacter enzymogenes

Authors

Yan Wang, University of Nebraska-Lincoln
Guoliang Qian, Nanjing Agricultural UniversityFollow
Yaoyao Li, Shandong University
Yansheng Wang, Nanjing Agricultural University
Yulan Wang, Nanjing Agricultural University
Stephen Wright, University of Nebraska-LincolnFollow
Yuezhong Li, Shandong University
Yuemao Shen, Shandong University
Fengquan Liu, Nanjing Agricultural UniversityFollow
Liangcheng Du, University of Nebraska-LincolnFollow

Date of this Version

6-2013

Citation

Wang Y, Qian G, Li Y, Wang Y, Wang Y, et al. (2013) Biosynthetic Mechanism for Sunscreens of the Biocontrol Agent Lysobacter enzymogenes. PLoS ONE 8(6): e66633. doi:10.1371/journal.pone.0066633

Comments

Copyright 2013 Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Abstract

Lysobacter are ubiquitous environmental bacteria emerging as novel biocontrol agents and new sources of anti-infectives. So far, very little effort has been invested in the study of the biology of these Gram-negative gliding bacteria. Many Lysobacter species are characterized by their yellow-orange appearance. Using transposon mutagenesis, we identified a stand-alone polyketide synthase (PKS) gene cluster required for the pigment production in L. enzymogenes OH11. The yellow pigments were abolished in the ‘‘white’’ mutants generated by target-specific deletions of ketosynthase (KS), acyl carrier protein, or ketoreductase. Spectroscopic data suggested that the pigments belong to xanthomonadin-like aryl polyenes. Polyene-type polyketides are known to be biosynthesized by modular PKS (Type I), not by stand-alone PKS (Type II) which always contain the heterodimer KS-CLF (chain-length factor) as the key catalytic component. Remarkably, this aryl polyene PKS complex only contains the KS (ORF17), but not the CLF. Instead, a hypothetical protein (ORF16) is located immediately next to ORF17. ORF16–17 homologs are widespread in numerous uncharacterized microbial genomes, in which an ORF17 homolog is always accompanied by an ORF16 homolog. The deletion of ORF16 eliminated pigment production, and homology modeling suggested that ORF16 shares a structural similarity to the N-terminal half of CLF. A point-mutation of glutamine (Q166A) that is the conserved active site of known CLF abolished pigment production. The ‘‘white’’ mutants are significantly more sensitive to UV/visible light radiation or H₂O₂ treatment than the wild type. These results unveil the first example of Type II PKS-synthesized polyene pigments and show that the metabolites serve as Lysobacter ‘‘sunscreens’’ that are important for the survival of these ubiquitous environmental organisms.