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ETH Zurich Research Collection Research Collection Doctoral Thesis Identification of Indigenous Phyllosphere Isolates of the Genus Sphingomonas as Plant-Protective Bacteria Author(s): Innerebner, Gerd Publication Date: 2011 Permanent Link: https://doi.org/10.3929/ethz-a-6620246 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library DISS. ETH NO. 19649 Identification of Indigenous Phyllosphere Isolates of the Genus Sphingomonas as Plant-Protective Bacteria A dissertation submitted to ETH Zurich for the degree of Doctor of Sciences Presented by Gerd Innerebner Mag. rer. nat., Leopold-Franzens-Universität Innsbruck Born on 3 January 1980 Citizen of Italy April 2011 Referees: Prof. Dr. Julia A. Vorholt Prof. Dr. Hans-Martin Fischer Prof. Dr. Leo Eberl Table of Contents Thesis Abstract ........................................................................................................................ 5 Zusammenfassung ................................................................................................................... 7 Chapter 1 General Introduction ............................................................................................................. 11 The phyllosphere as habitat for microorganisms ......................................................................... 11 Leaf-associated bacterial communities ......................................................................................... 11 Commensal, pathogenic, and beneficial bacteria ......................................................................... 13 Mechanisms of antagonism .......................................................................................................... 14 Biological control in the field ........................................................................................................ 16 Goals and outline of the thesis ..................................................................................................... 16 Chapter 2 Community proteogenomics reveals insights into the physiology of phyllosphere bacteria ................................................................................................................................. 21 Introduction .................................................................................................................................. 22 Results and Discussion .................................................................................................................. 22 Materials and Methods ................................................................................................................. 32 Supporting Information................................................................................................................. 34 Chapter 3 Sphingomonas strains protect Arabidopsis thaliana against leaf pathogenic Pseudomonas syringae in a controlled model system ............................................................. 55 Introduction .................................................................................................................................. 56 Materials and Methods ................................................................................................................. 56 Results ........................................................................................................................................... 60 Development of a gnotobiotic in planta assay ......................................................................... 60 Disease symptom development and pathogen proliferation in absence and presence of commensal bacteria .............................................................................................. 61 Screening of individual Sphingomonas isolates ........................................................................ 63 Carbon utilization profiles of Pst and representative Sphingomonas and Methylobacterium strains .................................................................................................. 64 Discussion ...................................................................................................................................... 65 Supplementary Figures ................................................................................................................. 68 Chapter 4 Studying possible mechanisms of antagonism in the plant-protective isolate Sphingomonas sp. Fr1 ............................................................................................................ 73 Introduction .................................................................................................................................. 73 Materials and Methods ................................................................................................................. 75 Results ........................................................................................................................................... 78 3 | P a g e Spatial distribution of Sphingomonas cells on leaf surfaces .................................................... 78 Proteome analysis of Sphingomonas sp. Fr1 ........................................................................... 81 Competition for nutrients ........................................................................................................ 83 Production of antimicrobial compounds ................................................................................. 85 Plant-mediated resistance ....................................................................................................... 86 Discussion ..................................................................................................................................... 88 Chapter 5 A forward genetic in planta screen to elucidate plant-protective traits of Sphingomonas sp. Fr1 ............................................................................................................. 93 Introduction ................................................................................................................................. 93 Materials and Methods ................................................................................................................ 94 Results .......................................................................................................................................... 97 Establishment of the screening procedure .............................................................................. 97 Realization of a screen with 1,500 Tn5 mutants ...................................................................... 99 Evaluation of Tn5 mutants in the microbox in planta assay .................................................. 100 Identification of the transposon insertion site in mutant GI1 ............................................... 101 In vitro inhibition assays ......................................................................................................... 102 Discussion ................................................................................................................................... 102 Chapter 6 General Discussion ............................................................................................................... 107 Community composition and physiology of phyllosphere bacteria .......................................... 107 Plant-protective bacteria ........................................................................................................... 108 Future perspectives .................................................................................................................... 109 Reference List ....................................................................................................................... 111 4 | P a g e Thesis Abstract Leaf surfaces are colonized by a large number and diversity of microorganisms. This habitat, also termed phyllosphere, represents one of the largest biological interphases on Earth and the indigenous microbiota is sufficiently large to have an impact on the global carbon and nitrogen cycles. It is thought that the majority of phyllosphere colonizers are commensal bacteria, which do not harm the plant. However, their role in this "harsh" environment, which is characterized by rapidly fluctuating conditions such as changes in temperature, UV radiation, and nutrient availability, is not clear. Here, complementary cultivation-independent methods were applied to study the composition and physiology of phyllosphere bacterial communities. Metagenomics and 16S rRNA gene based analysis revealed a high consistency of the leaf-associated microbiota on field-grown soybean, clover, and Arabidopsis thaliana plants. It was found that members of the alphaproteobacterial genera Methylobacterium and Sphingomonas were among the dominating bacteria in the phyllosphere. This was confirmed by community proteogenomics, which revealed also information about their physiology. Proteins of Methylobacterium were to a large extent related to C1 metabolism, whereas for Sphingomonas a remarkably high expression of transport-related proteins was observed. The predominance of these two commensal bacterial genera provoked the question about their role in the phyllosphere ecosystem. To investigate whether they support plants in defending pathogen attacks, a gnotobiotic in planta
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