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Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11

  • Genomics, transcriptomics, proteomics
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Abstract

Lysobacter enzymogenes is a bacterial biological control agent emerging as a new source of antibiotic metabolites, such as heat-stable antifungal factor (HSAF) and the antibacterial factor WAP-8294A2. The regulatory mechanism(s) for antibiotic metabolite biosynthesis remains largely unknown in L. enzymogenes. Clp, a cyclic adenosine monophosphate (cAMP)-receptor-like protein, is shown to function as a global regulator in modulating biocontrol-associated traits in L. enzymogenes. However, the genetic basis of Clp signaling remains unclear. Here, we utilized transcriptome/microarray analysis to determine the Clp regulon in L. enzymogenes. We showed that Clp is a global regulator in gene expression, as the transcription of 775 genes belonging to 19 functional groups was differentially controlled by Clp signaling. Analysis of the Clp regulon detected previously characterized Clp-modulated functions as well as novel loci. These include novel loci involved in antibiotic metabolite biosynthesis and surface motility in L. enzymogenes. We further showed experimentally that Clp signaling played a positive role in regulating the biosynthesis of HSAF and WAP-8294A2, as well as surface motility which is a type-IV-pilus-dependent trait. The regulation by Clp signaling of antibiotic (HSAF and WAP-8294A2) biosynthesis and surface motility was found to be independent. Importantly, we identified a factor Lysobacter acetyltransferase (Lat), a homologue of histone acetyltransferase Hpa2, which was regulated by Clp and involved in HSAF biosynthesis, but not associated with WAP-8294A2 production and surface motility. Overall, our study provided new insights into the regulatory role and molecular mechanism of Clp signaling in L. enzymogenes.

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Acknowledgments

We thank Dr. Robert Wilson Jackson from the University of Reading for critical revisions of this manuscript. We also thank Prof. Gary Y. Yuen from the University of Nebraska-Lincoln for technical support in surface motility. This study was supported by the National Natural Science Foundation of China (31371981), National Basic Research (973) program of China (2015CB150602) Program for New Century Excellent Talents in the University of Ministry of Education of China (NCET-13-0863), Fundamental Research Funds for the Central Universities (No. KYZ201205), Zhongshan Scholars of Nanjing Agricultural University, Special Fund for Agro-Scientific Research in the Public Interest (No. 201303015), the National High Technology Research and Development Program (“863” Program) of China (2011AA10A205), and Modern Agricultural Industry Technology System (No. CARS-29-09). The research in the Du lab is supported in part by the NIH (R01AI097260) and Nebraska Research Initiatives.

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Authors and Affiliations

  1. College of Plant Protection, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing Agricultural University, Nanjing, 210095, China

    Yansheng Wang, Yuxin Zhao, Juan Zhang, Yangyang Zhao, Yan Shen, Zhenhe Su, Gaoge Xu, Guoliang Qian & Fengquan Liu

  2. Institute of Plant Protection, Jiangsu Academy of Agricultural Science, Nanjing, 210014, People’s Republic of China

    Fengquan Liu

  3. Department of Chemistry, University of Nebraska—Lincoln, Lincoln, NE, 68588, USA

    Liangcheng Du

  4. Department of Chemistry, Pennsylvania State University-Penn State Altoona, Altoona, PA, 16601, USA

    Justin M. Huffman

  5. International Centre for Genetic Engineering and Biotechnology, Padriciano 99, 34149, Trieste, Italy

    Vittorio Venturi

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  1. Yansheng Wang
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  2. Yuxin Zhao
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  3. Juan Zhang
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  11. Guoliang Qian
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Correspondence to Guoliang Qian or Fengquan Liu.

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Wang, Y., Zhao, Y., Zhang, J. et al. Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11. Appl Microbiol Biotechnol 98, 9009–9020 (2014). https://doi.org/10.1007/s00253-014-6072-1

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