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Adaptive Strategies of Enterococcus Mundtii to Different Living Conditions in the Gut Microbiome of Spodoptera Littoralis Larvae

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Adaptive Strategies of Enterococcus Mundtii to Different Living Conditions in the Gut Microbiome of Spodoptera Littoralis Larvae Adaptive strategies of Enterococcus mundtii to different living conditions in the gut microbiome of Spodoptera littoralis larvae Dissertation To Fulfill the Requirements for the Degree of „doctor rerum naturalium“ (Dr. rer. nat.) Submitted to the Council of the Faculty of Biological Sciences of the Friedrich Schiller University Jena By Tilottama Mazumdar, Masters in Biotechnology, born on 17.04.1992 in India Reviewers 1. Prof. Dr. Wilhelm Boland, Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology 2. Prof. Dr. Erika Kothe, Institute of Microbiology, Friedrich Schiller University 3. Prof. Dr. David Heckel, Department of Entomology, Max Planck Institute for Chemical Ecology 4. Dr. Mark S Gresnigt, Leibniz Institute for Natural Product Research and Infection Biology – Hans Knöll Institute (HKI) 5. Prof. Dr. Dirk Hoffmeister, Leibniz Institute for Natural Product Research and Infection Biology – Hans Knöll Institute (HKI) 6. Prof. Dr. Dino McMahon, Institute of Biology – Zoology, Freie Universität Berlin Date of Defense- 19th November, 2020 2 “We are all of us walking communities of bacteria. The world shimmers, a pointillist landscape made of tiny living beings” --- Lynn Marguilis, Microcosmos: Four Billion Years of Microbial Evolution, 1986 “We can allow satellites, planets, suns, universe, nay whole systems of universe, to be governed by laws, but the smallest insect, we wish to be created at once by special act.” --- Charles Darwin, Darwin’s religious odessey, 2002 “Science cannot solve the ultimate mystery of nature. And that is because, in the last analysis, we ourselves are a part of the mystery that we are trying to solve.” --- Max Planck, Where is Science going? , 1981 3 Contents 1 Introduction .................................................................................................................................... 7 1.1 Symbiosis: How it all started ................................................................................................... 8 1.2 Hologenome theory of Evolution ............................................................................................ 9 1.2.1 Controversies about the hologenome theory .............................................................. 10 1.3 Colonization factors that influence the gut microbial population ........................................ 11 1.3.1 Colonization factors in insect guts ................................................................................ 13 1.4 Lepidoptera and their gut microbiota................................................................................... 15 1.5 The age of ‘Omics’ ................................................................................................................. 18 1.5.1 The practical applications of omics in insect-microbiome research. ............................ 20 2 Aims of the thesis .......................................................................................................................... 23 3 Overview of the chapters .............................................................................................................. 24 3.1 Chapter I ...................................................................................................................................... 24 3.2 Chapter II ..................................................................................................................................... 25 3.3 Chapter III .................................................................................................................................... 26 4 Chapter I ........................................................................................................................................ 28 The microbiome of Spodoptera littoralis: development, control and adaptation to the insect host .. 28 -A modified approach to study colonization strategies of symbionts in insect guts, in a real-time fashion ................................................................................................................................................... 28 4.1 Introduction ................................................................................................................................ 28 4.2 Fluorescent reporters and its applications in in vivo imaging .................................................... 30 4.2.1 Fluorescent proteins ............................................................................................................ 31 4.2.2 Construction of a GFP fluorescent system for E. mundtii .................................................... 31 4.2.3 Transformation of E. mundtii KD251 using electroporation ................................................ 33 4.2.4 Colonization of GFP-tagged bacterium in the gut of S. littoralis ......................................... 34 4.3 Fluorescent-activated cell sorting ............................................................................................... 35 4.4 RNA extraction ............................................................................................................................ 36 4.5 Transcriptomics ........................................................................................................................... 38 4.5.1 RNASeq ................................................................................................................................. 39 4.5.2 Adaptation and survival strategies of E. mundtii in the gastro-intestinal of insect ............. 42 4.6 Discussion and future prospects ................................................................................................. 46 5 Chapter II ....................................................................................................................................... 49 Transcriptomics reveal the survival strategies of Enterococcus mundtii in the gut of Spodoptera littoralis ................................................................................................................................................. 49 4 5.1 Introduction ................................................................................................................................ 50 5.2 Results ......................................................................................................................................... 51 5.2.1 Sorting of GFP-tagged E. mundtii cells from the gut of experimentally colonized S. littoralis larvae by flow cytometry .............................................................................................................. 52 5.2.2 RNAseq analysis revealed many differentially expressed genes between E. mundtii growing in vitro vs. in vivo ........................................................................................................... 52 5.2.3 Gene enrichment analysis revealed several pathways differentially expressed between E. mundtii growing in vitro vs. in vivo ............................................................................................... 55 5.2.4 Survival strategies of E. mundtii in the gut of S. littoralis .................................................... 58 5.3 Discussion .................................................................................................................................... 62 5.4. Materials and methods .............................................................................................................. 68 6 Chapter III ...................................................................................................................................... 72 Role of 8-Hydroxyquinoline-2-carboxylic acid in defining the bacterial landscape in the guts of Spodoptera littoralis larvae ................................................................................................................... 72 6.1 Introduction ................................................................................................................................ 72 6.2 Materials and Methods ............................................................................................................... 74 6.3 Results ......................................................................................................................................... 77 6.3.1. 8-HQA measurements in KMO-knockouts as compared to WT larvae ............................... 77 6.3.2. Microbial diversity in WT and KMO knockouts across the life stages of S. littoralis .......... 78 6.3.3Levels of the most abundant taxa along the developmental stages .................................... 80 6.3.4. Alpha and Beta diversity analysis ........................................................................................ 81 6.4 Discussion .................................................................................................................................... 85 7 General Discussion ........................................................................................................................ 87 7.1 Reporter technology and advancements .............................................................................. 87 7.2 Reporter gene and bio reporter technology in our research ............................................... 88 7.3 Flow cytometry making its way in host-symbiont research ................................................. 89 7.4 Enterococcus mundtii in the fore and hind guts of Spodoptera littoralis larvae .................. 91 7.5 Host genetic control
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