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Actinobacteria and the Vitamin Metabolism of Firebugs

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Actinobacteria and the Vitamin Metabolism of Firebugs Actinobacteria and the Vitamin Metabolism of Firebugs - Characterizing a mutualism's specificity and functional importance - Seit 1558 Dissertation To Fulfill the Requirements for the Degree of „Doctor of Philosophy“ (PhD) Submitted to the Council of the Faculty of Biology and Pharmacy of the Friedrich Schiller University Jena by M.S. Hassan Salem Born on 16.01.1986 in Cairo, Egypt i Das Promotionsgesuch wurde eingereicht und bewilligt am: Gutachter: 1) 2) 3) Das Promotionskolloquium wurde abgelegt am: ii To Nagla and Samy, for ensuring that life’s possibilities remain endless To Aly, for sharing everything* And to Aileen, my beloved HERC2 mutant * Everything except our first Gameboy (circa 1993). For all else, I am profoundly grateful. i ii CONTENTS LIST OF PUBLICATIONS ................................................................................................... 1 CHAPTER 1: SYMBIOSIS AND THE EVOLUTION OF BIOLOGICAL NOVELTY IN INSECTS ............................................................................................................................ 3 1.1 The organism in the age of the holobiont: It, itself, they .................................................. 3 1.2 Adaptive significance of symbiosis .................................................................................. 4 1.3 Symbiont-mediated diversification ................................................................................... 5 1.4 Revisiting Darwin’s mystery of mysteries: The role of symbiosis in species formation 6 1.5 Homeostasis of symbioses ................................................................................................ 8 1.6 The Pyrrhocoridae-Actinobacteria symbiosis................................................................. 10 1.6.1 Hemiptera: Pyrrhocoridae ........................................................................................ 10 1.6.2 Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs ...................... 10 1.7 Thesis outline .................................................................................................................. 12 1.8 References ....................................................................................................................... 13 CHAPTER 2: AN OUT-OF-BODY EXPERIENCE: THE EXTRACELLULAR DIMENSION FOR THE TRANSMISSION OF MUTUALISTIC BACTERIA IN INSECTS ................................................................................................................................ 18 2.1 Abstract ........................................................................................................................... 18 2.2 Introduction ..................................................................................................................... 19 2.3 Overview of extracellular transmission routes of insect symbionts ............................... 20 2.3.1 Environmental determination .................................................................................. 22 2.3.2 Coprophagy .............................................................................................................. 23 2.3.3 Social acquisition ..................................................................................................... 23 2.3.4 Egg and oviposition site inoculation ........................................................................ 25 2.3.5 Capsule transmission ............................................................................................... 25 2.3.6 Milk gland secretions ............................................................................................... 26 2.4 Evolution of mutualistic associations ............................................................................. 27 2.5 Evolutionary transitions among transmission routes ...................................................... 29 2.6 Implications for symbiont genome evolution ................................................................. 30 2.7 Host-symbiont evolutionary dynamics .......................................................................... 35 2.8 Conclusions and future perspectives .............................................................................. 36 2.9 Acknowledgments ......................................................................................................... 37 2.10 References .................................................................................................................... 38 2.10 Supplement .................................................................................................................. 45 i CHAPTER 3: GEOGRAPHIC AND ECOLOGICAL STABILITY OF THE SYMBIOTIC MID-GUT MICROBIOTA IN EUROPEAN FIREBUGS, PYRRHOCORIS APTERUS (HEMIPTERA, PYRRHOCORIDAE) ............................... 57 3.1 Abstract ........................................................................................................................... 57 3.2 Introduction ..................................................................................................................... 58 3.3 Materials and methods .................................................................................................... 60 3.3.1 Rearing conditions and sample collection .............................................................. 60 3.3.2 DNA extraction and amplification ........................................................................... 61 3.3.3 Bacterial tag-encoded FLX amplicon pyroseqencing (bTEFAP) ............................ 61 3.3.4 PCR amplification, cloning, and sequencing .......................................................... 61 3.3.5 Molecular phylogenetic analysis ............................................................................. 62 3.3.6 Quantitative PCR ..................................................................................................... 62 3.3.7 Fluorescence in-situ hybridization (FISH) .............................................................. 63 3.3.8 Microelectrode measurements ................................................................................. 64 3.4 Results............................................................................................................................. 64 3.4.1 Bacterial communities in different gut regions of P. apterus ................................. 64 3.4.2 Phylogenetic placement of P. apterus midgut symbionts ....................................... 66 3.4.3 Ontogenetic changes of the P. apterus microbiota .................................................. 67 3.4.4 Inter-population differences in the mid-gut microbiota of P. apterus ..................... 69 3.4.5 Effect of different diets on the mid-gut microbiota of P. apterus ........................... 69 3.4.6 Transient microbes from ingested food material ..................................................... 70 3.4.7 Localisation of microbial symbionts ........................................................................ 71 3.4.7 Microelectrode measurements ................................................................................. 71 3.5 Discussion ....................................................................................................................... 72 3.5.1 Composition of the P. apterus gut microbiota ......................................................... 72 3.5.2 Transmission and establishment of the microbial mid-gut community ................... 73 3.5.3 Ecological stability of the P. apterus gut microbiota .............................................. 73 3.5.4 Comparison of methods for the characterization of microbial communities ........... 74 3.5.5 Putative function of the P. apterus mid-gut microbiota .......................................... 75 3.6 Acknowledgments ......................................................................................................... 76 3.7 References ....................................................................................................................... 77 3.8 Supplement ..................................................................................................................... 85 CHAPTER 4: ACTINOBACTERIA AS ESSENTIAL SYMBIONTS IN FIREBUGS AND COTTON STAINERS (HEMIPTERA, PYRRHOCORIDAE) .............................. 89 4.1 Abstract ........................................................................................................................... 89 4.2 Introduction ..................................................................................................................... 90 4.3 Results ............................................................................................................................ 91 ii 4.3.1 Midgut microbiota of D. fasciatus ........................................................................... 91 4.3.2 Success of symbiont manipulation procedure.......................................................... 92 4.3.3 Fitness of P. apterus and D. fasciatus following symbiont manipulation ............... 94 4.3.4 Reproductive success of adult D. fasciatus females following symbiont manipulation .................................................................................................................... 95 4.3.5 Correlations linking individual strain abundances to fitness ................................... 96 4.3.6 Fitness of D. fasciatus fed on sunflower seeds ........................................................ 98 4.4 Discussion ......................................................................................................................
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