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Genome, Mutational and RNA-Seq Analyses of Janthinobacterium And Genome, mutational and RNA-seq analyses of Janthinobacterium and Duganella strains reveal the presence of a single α-hydroxyketone-like quorum sensing system involved in bacterial-fungal interactions Dissertation for obtaining the degree Doctor rerum naturalium (Dr. rer. nat.) at the Department of Biology Subdivision of the Faculty of Mathematics, Informatics and Natural Sciences of the University of Hamburg by Frederike Svenja Haack from Itzehoe Hamburg 2016 Approved by the Department of Biology, University of Hamburg at the request of Prof. Dr. Wolfgang Streit Second evaluator of the dissertation: Prof. Dr. Wilhelm Schäfer Date of defense (Disputation): 24. October 2016 This is a corrected version. Declaration on oath I hereby declare, on oath, that I have written the present dissertation by my own and have not used other than the acknowledged resources and aids. Hamburg, ______________________________ Frederike Haack English Language Declaration I hereby declare as a native English speaker that I have checked the thesis “Genome, mutational and RNA-seq analyses of Janthinobacterium and Duganella strains reveal the presence of a single α-hydroxyketone-like quorum sensing system involved in bacterial-fungal interactions” by Frederike Svenja Haack for grammatically correct English and the scientific accuracy of the language. I also confirm that I am a native English speaker. Sincerely, _________________________________ Carla Haslauer Following publications contribute to this research Frederike S. Haack, Anja Poehlein, Cathrin Kröger, Christian A. Voigt, Meike Piepenring, Helge B. Bode, Rolf Daniel, Wilhelm Schäfer and Wolfgang R. Streit (2016). „Molecular Keys to the Janthinobacterium and Duganella spp. Interaction with the Plant Pathogen Fusarium graminearum”. Front. Microbiol. 7:1668. doi: 10.3389/fmicb.2016.01668 Claudia Hornung, Anja Poehlein, Frederike S. Haack, Martina Schmidt, Katja Dierking, Andrea Pohlen, Hinrich Schulenburg, Melanie Blokesch, Laure Plener, Kirsten Jung, Andreas Bonge, Ines Krohn-Molt, Christian Utpatel, Gabriele Timmermann, Eva Spieck, Andreas Pommerening-Röser, Edna Bode, Helge B. Bode, Rolf Daniel, Christel Schmeisser and Wolfgang R. Streit (2012). “The Janthinobacterium sp. HH01 genome encodes a homologue of the V. cholerae CqsA and L. pneumophila LqsA autoinducer synthases”. PLoS One. 8(2): e55045. doi: 10.1371/journal.pone.0055045 Table of content I Table of content Table of content ........................................................................................................... I Figures ....................................................................................................................... IV Tables ......................................................................................................................... VI 1 Introduction ...................................................................................................... 1 1.1 The family Oxalobacteraceae ............................................................................. 1 1.1.1 The genus Janthinobacterium ............................................................................ 1 1.1.2 The genus Duganella ......................................................................................... 2 1.2 Janthinobacterium and Duganella interact with eukaryotes ................................ 3 1.2.1 Bacterium-fungus interaction .............................................................................. 3 1.2.2 Oxalobacteraceae-fungus interaction ................................................................. 4 1.3 Bacterial communiation – quorum sensing ......................................................... 6 1.4 How bacteria talk – the language ....................................................................... 7 1.5 Using α-hydroxyketones for bacterial communication ......................................... 9 1.6 Intention of this work ........................................................................................ 12 2 Material and methods ..................................................................................... 13 2.1 Bacterial strains ................................................................................................ 13 2.2 Vectors and constructs ..................................................................................... 14 2.3 Primer .............................................................................................................. 15 2.4 Bacterial cultivation .......................................................................................... 16 2.5 Violacein measurement .................................................................................... 17 2.6 Bacterial characterization ................................................................................. 17 2.6.1 Growth conditions ............................................................................................. 18 2.6.2 Hydrolytic and chitin degradation activities ....................................................... 18 2.7 Phylogenetic classification and genome analyses ............................................ 19 2.7.1 16S rRNA analysis ........................................................................................... 19 2.7.2 Whole genome sequencing .............................................................................. 20 2.7.3 Comparative genomics ..................................................................................... 20 2.8 Mutagenesis of Janthinobacterium sp. HH102 ................................................. 21 2.8.1 Generating a jqsA gene deletion mutant ........................................................... 21 2.8.2 Complementation of the jqsA gene deletion mutant .......................................... 22 2.8.3 Identification of JAI-1 ........................................................................................ 23 2.9 RNA-seq analyses ............................................................................................ 23 2.9.1 RNA analyses of HH01 and HH01ΔjqsA in late stationary phase ..................... 23 2.9.2 RNA analyses of HH01, HH01ΔjqsA, HH102 and HH102ΔjqsA in early stationary phase ............................................................................................... 24 2.9.3 Quantitative real time PCR ............................................................................... 25 2.10 Promoter-fusion studies .................................................................................... 26 Table of content II 2.11 Coincubation studies of bacteria and fungi ....................................................... 27 2.11.1 Plate assay of Janthinobacterium or Duganella with Fusarium graminearum ... 27 2.11.2 Liquid assay of Janthinobacterium or Duganella with Fusarium graminearum .................................................................................................... 28 3 Results ............................................................................................................ 29 3.1 Isolates are affiliated with the family Oxalobacteraceae .................................... 29 3.1.1 Morphology ...................................................................................................... 29 3.1.2 Phylogenetic classification ................................................................................ 32 3.1.2.1 16S rRNA gene analyses ................................................................................. 32 3.1.2.2 Phylogenetic classification according to comparative genomics ....................... 33 3.2 Physiological characterization of the isolates .................................................... 38 3.2.1 Bacterial growth ................................................................................................ 38 3.2.2 Secondary metabolite synthesis ....................................................................... 40 3.2.3 Hydrolytic activity .............................................................................................. 40 3.2.4 Protein translocation ......................................................................................... 42 3.3 Oxalobacteraceae isolates inhibit the growth of the fungus Fusarium graminearum .................................................................................................... 45 3.3.1 Oxalobacteraceae inhibit fungal growth ............................................................ 46 3.4 Despite phylogenetical differencies, various Oxalobacteraceae harbor functional homologues of the JQS system ........................................................ 48 3.4.1 The JQS system ............................................................................................... 49 3.4.2 Phenotypical impact of JAI-1 on HH102 ........................................................... 52 3.4.3 CAI-1 and LAI-1 complement a jqsA gene deletion of OxaI and OxaII representatives ................................................................................................. 54 3.4.4 Clues to the possible JAI-1 structure ................................................................ 56 3.5 RNA-seq analyses reveal the regulation of nine distinct gene clusters of HH01 and HH102 ............................................................................................. 59 3.5.1 JAI-101 influences the secondary metabolite and lipopolysaccharide synthesis .........................................................................................................
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