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Research Collection Research Collection Doctoral Thesis In search of symbiotically relevant genes of Bradyrhizobium japonicum Author(s): Murset, Valérie Publication Date: 2012 Permanent Link: https://doi.org/10.3929/ethz-a-007605200 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. 20886 In search of symbiotically relevant genes of Bradyrhizobium japonicum A dissertation submitted to the ETH Zurich for the degree of DOCTOR OF SCIENCES presented by VALERIE MURSET MSc in Genomics and Experimental Biology, University of Lausanne Born on June 27th, 1986 citizen of Twann, BE Accepted on the recommendation of: Prof. Dr. Hauke Hennecke, examiner Dr. Gabriella Pessi, co-examiner Prof. Dr. Dieter Haas, co-examiner Prof. Dr. Enrico Martinoia, co-examiner 2012 Table of contents Thesis summary 1 Résumé 3 Chapter 1: Introduction 7 Rhizobia and agriculture 8 Bradyrhizobium japonicum 10 Nodulation process 11 Nod factors 11 Type III secretion system (T3SS) 12 Nodule organogenesis and bacterial infection 13 Symbiotic nitrogen fixation 15 Transcriptional regulation of nitrogen fixation genes 17 Nodule metabolism 20 Symbiotically relevant genes 22 Aim of this work 23 Chapter 2: Genes potentially important for symbiosis: σ54- and NifA-dependent genes 25 Abstract 26 Introduction 27 Materials and methods 29 Bacterial strains, media and growth conditions 29 DNA methods and construction of blr2131, blr2135, blr1765, bll1767 mutant strains 29 Plant material, inoculation and cultivation 32 Results 33 Characterization and transcription analysis of the blr2131-2136 genomic region 33 Characterization and transcription analysis of blr1765 and bll1767 36 Discussion 39 Chapter 3: Disparate role of rhizobial ACC deaminase in root-nodule symbioses 41 Abstract 42 Introduction 43 Materials and methods 45 Bacterial strains, media and growth conditions 45 DNA methods and construction of blr0241 mutant strains 45 Plant material, inoculation, and growth conditions 46 ACC deaminase activity assay 46 Results and Discussion 47 A survey on the occurrence and function of the ACC deaminase gene (acdS) in the Rhizobiales 47 Analysis of the B. japonicum acdS genomic region 50 Construction and phenotypical analysis of a B. japonicum ACC deaminase mutant 52 B. japonicum ACC deaminase activity assay 54 Concluding remarks 56 Acknowledgments 57 Chapter 4: B. japonicum-specific adaptations to the host 59 Abstract 60 Introduction 61 Rhizobial adaptation to the host 61 B. japonicum-specific adaptation to cowpea 62 Further investigation of the B. japonicum host-specific adaptation concept using nodule metabolomics 63 Materials and methods 65 Bacterial strains, media and growth conditions 65 DNA methods and construction of bll0342-bll0343 mutant strains 65 Plant material, inoculation and cultivation 67 Isothermal calorimetry 67 Metabolomics of nodules 67 Results 69 Cowpea-specific adaptation genes of B. japonicum involved in tyrosine degradation 69 Metabolomics of nodules 74 Comparison between wild-type nodules from the different host plants 74 Comparison between wild-type and mutant nodules 78 Discussion 79 Chapter 5: Copper-responsive transcriptional regulation in B. japonicum 83 Abstract 84 Introduction 85 Materials and methods 89 Bacterial strains, media and growth conditions 89 DNA methods and construction of bsr0701 mutant strains 89 Plant material, inoculation and cultivation 94 RNA isolation and synthesis of cDNA 94 Quantitative Real-Time PCR 94 Microarray experiment and analysis 94 Primer extension 95 Construction of lacZ fusions, and β-galactosidase assay 95 Results 97 Study of the transcriptional regulation of the pcuABCDE operon 97 Identification of bsr0701, a CsoR homolog 100 Construction and characterization of bsr0701 deletion strains 100 Determination of the bsr0701 regulon 105 Discussion 109 Chapter 6: Future perspectives 112 Genes potentially important for symbiosis: σ54- and NifA-dependent genes 113 blr2131-2136, blr1765 and bll1767 113 blr0241, the ACC deaminase gene 113 Survey on all the NifA-regulated genes mutated in B. japonicum 114 B. japonicum-specific adaptations to the host 116 Copper-responsive transcriptional regulation in B. japonicum 117 Bibliography 118 Supplementary Material 127 Publications 128 Curriculum vitae 129 Acknowledgments 130 Summary Thesis summary Bradyrhizobium japonicum is a soil bacterium with the ability to infect roots of leguminous plants such as soybean, cowpea, mungbean, and siratro and induce the formation of a novel plant organ, the nodule. In the symbiotic state, the bacteria differentiate into bacteroids that are capable of fixing atmospheric nitrogen into ammonia. This source of nitrogen is used by the host plant and promotes its growth. In return, the bacteroids are supplied with an environment rich in carbon generated by the plant via photosynthesis. Symbiotic nitrogen fixation is an important component of the nitrogen cycle. The first part of this thesis is dedicated to the characterization of potentially new functions essential in symbiosis. Strict criteria were applied for candidate gene selection: up-regulation in symbiosis compared to free- living conditions, a NifA- and RpoN-dependent expression, and protein detection in bacteroids. Four genes were chosen for characterization through mutant construction: two genes (blr2131, blr2135) that are part of an operon of unknown function (blr2131-2136), a ferredoxin gene (blr1765), and a gene coding for a hypothetical protein (bll1767); the latter two are located in the nitrogenase gene cluster. Despite the careful choice of candidate genes, no relevant phenotypes could be observed for any of the mutants of these genes. In the third chapter, I focused on the characterization of the B. japonicum 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (blr0241), which is also a NifA- and RpoN-regulated gene. ACC deaminases had been shown to protect rhizobia against the inhibitory effects of ethylene produced by the host plant during the nodulation process. This enzyme converts ACC, a precursor of the plant hormone ethylene, into ammonia and α-ketobutyrate. In free-living, wild-type B. japonicum an ACC deaminase activity could be measured, whereas a blr0241 mutant did not show any enzymatic activity. However, the mutant was not impaired in its ability to nodulate soybean, cowpea, siratro, and mungbean. Also, the blr0241 mutant strain was not affected in its competitiveness for nodulation and nodule occupation compared to the wild-type strain. These results suggested that the role of B. japonicum ACC deaminase differs from that in other rhizobial-plant interactions investigated. In the fourth chapter, the host-specific adaptation of B. japonicum to cowpea was studied. A previous report had revealed that genes coding for enzymes of the tyrosine degradation pathway are specifically up-regulated in cowpea bacteroids compared to soybean and siratro bacteroids, and the products of these genes are exclusively found in cowpea bacteroids (Koch et al. 2010). To study the possible importance of this pathway in B. japonicum, deletion mutations in the fumarylacetoacetase (bll0342) and homogentisate 1,2-dioxygenase (bll0343) genes were constructed. The mutants showed no symbiosis phenotype on all host plants tested. We 1 Summary could prove that B. japonicum wild type and the Δbll0342-bll0343 mutant were able to grow on plates with tyrosine as sole C-source, leading to the hypothesis that B. japonicum may have a bypass pathway for tyrosine degradation. In addition, and in order to possibly add new information to the host specificity concept, the metabolome of soybean, cowpea, mungbean and siratro nodules was determined, which showed striking differences. This study may lead to a better understanding of nodule metabolism and of bacterial-specific adaptation to the host. Since the initial goal of my thesis could not be reached, namely the characterization of new functions involved in symbiosis, we decided to terminate the projects so far described. In the last part of my doctoral work, I focused on a new research area, the characterization of B. japonicum copper-responsive transcriptional regulators. First, the transcriptional regulation of the pcuABCDE operon that had been shown to be involved in copper trafficking was studied. The expression of the pcuA and pcuB genes was shown by qRT-PCR to be up-regulated in copper-limited conditions compared to normal copper conditions. The mapping of the pcuABCDE promoter region did not allow the identification of regulatory elements interacting with the pcuABCDE promoter. A homology search for conserved copper-responsive transcriptional regulators in the B. japonicum genome was then performed. A homolog of the transcriptional repressor CsoR (bsr0701) was detected and characterized. Bsr0701 deletion mutants showed a strong growth delay in anoxic, denitrifying conditions. In symbiosis only one of the two mutants (kanamycin resistance cassette in opposite orientation) showed a strong phenotype which we could not explain. The Bsr0701 regulon was determined by microarray analysis. 2 Résumé Résumé Bradyrhizobium japonicum est une bactérie capable d'induire la formation d'organes particuliers, les nodules, sur les racines des plantes de la famille des légumineuses tels que le soja, le haricot mungo, le siratro et le niébé. Dans le nodule, les bactéries se différencient en bactéroïdes capables
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