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Symbiotic Specificity and Nodulation in the Southern African Legume Clade Lotononis S

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Symbiotic Specificity and Nodulation in the Southern African Legume Clade Lotononis S Symbiotic specificity and nodulation in the southern African legume clade Lotononis s. l. and description of novel rhizobial species within the Alphaproteobacterial genus Microvirga by Julie Kaye Ardley This thesis is presented for the degree of Doctor of Philosophy of Murdoch University 2011 DECLARATION I declare that this thesis is my own account of my research and contains as its main content work which has not previously been submitted for a degree at any tertiary education institution. Julie Kaye Ardley ii TABLE OF CONTENTS Publications arising from this thesis………………………………………………….ix Acknowledgements……………………………………………………………………………x Abstract…………………………………………………………………………………………..xii Chapter 1: Introduction and literature review……………………………………1 1.1 The legume-rhizobia symbiosis….……………….…….……………………………………..………..3 1.2 The legume-rhizobia symbiosis in Australian agriculture.………………………….……….4 1.2.1 Background…………………………………………………………………………………….…….…..4 1.3 Legumes.……….……………………………………………………………………………………..……….….6 1.3.1 Evolution of legumes…………………………………………….……….…………….…….…….6 1.3.2 Legume taxonomy and phylogeny………………………………………………….…………7 1.3.2.1 Phylogeny of the Papilionoideae…………………………….………….…………..….8 1.4 Rhizobia…..…………………………………………………………………….………………………………..11 1.4.1 History of rhizobial classification……………………………………………………...……..11 1.5 Bacterial systematics….……………………….…………….………………………………….….……..13 1.5.1 Genotypic classification methods………………………………………………..…….……15 1.5.2 Phylogenetic classification methods…………………..…………………..………….…..15 1.5.3 Phenotypic classification methods………………………………………..…..…………...18 1.5.4 The effect of lateral gene transfer on bacterial phylogeny…………………...…19 1.6 General recommendations for classifying and describing bacteria……….………….21 1.7 Rhizobial symbiotic genes………………………………………………………..………………………23 1.7.1 The role of nodulation genes and Nod factors…………………………………………24 1.8 Rhizobial infection and nodule formation in legumes………………………………………25 1.8.1 Infection pathways in legumes……………………………..…………………………….…..26 iii 1.8.2 Nodule types………………………………………………………..……………………….………..29 1.8.2.1 Formation and structure of nodules infected via infection threads………………………………………………………………………………………….…….……….30 1.8.2.2 Formation and structure of intercellularly infected nodules …………….31 1.9 Specificity and effectiveness in the legume-rhizobia symbiosis………………………..32 1.10 The Lotononis s. l. clade………………………………………………………………………………...34 1.10.1 The genus Listia …………………………………………………………………………………....36 1.10.2 The genus Leobordea …………………………………………………………………….………37 1.10.3 The genus Lotononis s. str ……………………………………………………………………..38 1.11. The Lotononis s. l. -rhizobia symbiosis…………………………………………………………..39 1.12 Summary of current knowledge of the symbiotic relationships between Lotononis s. l . and associated rhizobia……………………………………………………………………44 1.13 Aims of this thesis…………………………………………………………………………………….……46 Chapter 2: Determining symbiotic specificity within Lotononis s.l. …. 47 2.1 Introduction…………………………………………………………………………………………………….49 2.1.1 Background……………………………………………………………………………………………..49 2.1.2 Experimental approach……………………………………………………………………………50 2.2 Materials and methods…………………………………………………………………………………...53 2.2.1 Rhizobial strains………………………………………………………………………………………53 2.2.2 Host plants………………………………………………………………………………………………53 2.2.3 Glasshouse experimental design……………………………………………………………..55 2.2.4 General glasshouse procedures……………………………………………………………….58 2.2.4.1 Preparation of plant material……………………………………………………………59 2.2.4.2 Preparation of inoculum……………………………………………………………………60 2.2.4.3 Harvesting…………………………………………………………………………………………61 2.2.5 Statistics………………………………………………………………………………………………….61 2.2.6 Molecular fingerprinting………………………………………………………………………….61 2.2.7 Amplification and sequencing of 16S rRNA genes……………………………………63 2.2.8 Amplification and sequencing of nodA genes………………………………………….66 2.3 Results……………………………………………………………………………………………………………..68 iv 2.3.1 Selection of inoculant strains………………………………………………………………..…68 2.3.1.1 Selection of a representative Listia angolensis strain………………...……..68 2.3.1.2 Authentication of non-pigmented Lotononis s. l. strains……………………69 2.3.2 Symbiotic interactions of Lotononis s. l. species with phylogenetically diverse Lotononis s. l. rhizobia………………………………………………………………………….71 2.3.3 Symbiotic specificity within Listia species………………………………………………..75 2.3.4 Nodule structure in Lotononis s. l. species……………………………………………….75 2.3.5 Amplification and sequencing of 16S rRNA genes……………………………………77 2.3.6 Amplification and sequencing of nodA …………………………………………………….84 2.3.6.1 nodA sequences of WSM2598 and WSM2667…………………………………..84 2.3.6.2 nodA sequences of the remaining Lotononis s. l. rhizobia…………………85 2.4 Discussion………………………………………………………………………………………………………..90 2.4.1 Nodule structure in Lotononis s. l. species……………………………………………….90 2.4.2. Diversity of Lotononis s. l. rhizobia………………………………………………………….90 2.4.2 1 The Methylobacterium lineage………………………………………………………….91 2.4.2.2 The Microvirga lineage……………………………………………………………………..93 2.4.2.3 The Bradyrhizobium , Ensifer and Mesorhizobium lineages…………….….94 2.4.3 Symbiotic relationships within Lotononis s. l. hosts………………………………...96 2.4.4 Phylogeny of nodA genes…………………………………………………………………………98 2.4.5 Environmental factors that may be effectors of diversification in rhizobia associated with Lotononis s. l. species……………………………………………………………103 2.4.6 Putative evolution of symbiotic patterns within Lotononis s. l. …………….107 Chapter 3 Nodule structure in Lotononis s. l. species and infection and nodule formation in Listia angolensis and Listia bainesii …………….….111 3.1 Introduction…………………………………………………………………………………………………..113 3.1.1 Modes of infection and nodulation in legumes……………………………………..113 3.2 Materials and methods………………………………………………………………………………….115 3.2.1 Legume hosts, bacterial inoculant strains and growth conditions………….115 3.2.2 Harvesting……………………………………………………………………………………………..117 3.2.3 Nodule initial staining and sectioning, nodule sectioning and light microscopy…………………………………………………………………………………………………....118 v 3.3 Results……………………………………………………………………………………………………………119 3.3.1. Localisation of infection site…………………………………………………………………119 3.3.2 Infection and nodule organogenesis in Listia angolensis and Listia bainesii …………………………………………………………………………………………………………..121 3.3.3 Localisation of the infection site in Listia angolensis and Listia bainesii plants inoculated at 85 days old…………………………………………………………………….124 3.3.4 Internal structure of Lotononis s. l. nodules…………………………………………..125 3.4 Discussion………………………………………………………………………………………………………128 Chapter 4 Characterisation and description of novel Listia angolensis and Lupinus texensis rhizobia……………………………………..…………………133 4.1 Introduction…………………………………………………………………………………………………..135 4.2 Materials and methods………………………………………………………………………………….137 4.2.1 Bacterial strains and culture conditions…………………………………………………137 4.2.2 DNA amplification and sequencing………………………………………………………..137 4.2.2.1 Amplification and sequencing of the 16S rRNA gene………………………137 4.2.2.2 Amplification and sequencing of the nodA gene…………………………….139 4.2.3 Phenotypic characterisation………………………………………………………………….139 4.2.3.1 Morphology…………………………………………………………………………………….139 4.2.3.2 Extraction of pigments……………………………………………………………………140 4.2.3.3 Temperature range…………………………………………………………………………141 4.2.3.4 Optimal growth temperature………………………………………………………….141 4.2.3.5 Growth curves and determination of mean generation time………….141 4.2.3.6 Determination of sodium chloride and pH tolerance………………………141 4.2.3.7 Anaerobic growth……………………………………………………………………………143 4.2.3.8 Antibiotic sensitivity……………………………………………………………………….143 4.2.3.9 Substrate utilisation………………………………………………………………………..144 4.2.3.9.1 Utilisation of sole carbon sources in Biolog GN2 plates…………….144 4.2.3.9.2 Utilisation of substrates in Biolog Phenotype Microarray plates……………………………………………………………………………………………………..144 4.2.3.9.3 Growth on sole carbon substrates……………………………………………145 4.2.3.10 Biochemical characterisation………………………………………………………..147 vi 4.2.4 Host range…………………………………………………………………………………………….148 4.3 Results……………………………………………………………………………………………………………149 4.3.1 Amplification and sequencing of the 16S rRNA gene……………………………..149 4.3.2 Amplification and sequencing of nodA …………………………………………………..151 4.3.3 Phenotypic characterisation………………………………………………………………….153 4.3.3.1 Morphology…………………………………………………………………………………….153 4.3.3.2 Characterisation of pigments………………………………………………………….155 4.3.3.3 Growth characteristics……………………………………………………………………156 4.3.3.4 Antibiotic sensitivity……………………………………………………………………….156 4.3.3.5 Substrate utilisation………………………………………………………………………..158 4.3.3.5.1 Utilisation of sole carbon sources in Biolog GN2 plates…………….158 4.3.3.5.2 Utilisation of substrates in Biolog Phenotype Microarray plates………………………………………………………………………………………………………162 4.3.3.5.3 Growth in sole carbon substrate broths……………………………………168 4.3.3.6 Biochemical characterisation………………………………………………………….169 4.3.4 Host range…………………………………………………………………………………………….171 4.4 Discussion………………………………………………………………………………………………………173 4.4.1 Genotypic characterisation of novel Microvirga species………………………..173 4.4.2 G+C content, DNA:DNA hybridisation and cellular fatty acid analysis…….176 4.4.3 Phenotypic characterisation of novel Microvirga species………………………176 4.4.3.1 Substrate utilisation………………………………………………………………………..181 4.4.3.1.1 Critique of the use of Biolog plates in determining substrate utilisation………………………………………………………………………………………………..181 4.4.3.1.2 Substrate utilisation in Listia angolensis and Lupinus texensis strains
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