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Characteristics of Genome Evolution in Obligate Insect Symbionts, Including The Characteristics of genome evolution in obligate insect symbionts, including the description of a recently identified obligate extracellular symbiont. Thesis Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Laura Jean Kenyon, B.S. Graduate Program in Evolution, Ecology, and Organismal Biology The Ohio State University 2015 Thesis Committee: Norman Johnson Andy Michel Kelly Wrighton Zakee L. Sabree, Advisor Copyright by Laura Jean Kenyon 2015 Abstract Animal-bacterial symbioses have shaped the evolution of all eukaryotic organisms. All symbioses have in common a long-term association and therefore provide valuable insight into the evolution and diversification of both partners. Insect-bacterial mutualisms represent the most extreme natural partnerships known, showing evidence of coevolution and obligate interdependence between the partners. Early investigations of plant sap-feeding insects, in particular, revealed tissues of unknown function inhabited by bacteria and insects void of their symbionts revealed reduced host fitness compared to symbiotic insects. Due to the obligate nature of the relationships, endosymbiotic bacteria are uncultivable, but complete genome sequencing suggests bacterial mutualists metabolic capabilities and likely contribution to the mutualisms, typically nutrient provisioning. A well-supported pattern of bacterial genome evolution for obligate mutualists is extreme genome reduction, likely due to relaxed selection upon genes that are not required in the stable environment of the host, leading to an accumulation of deleterious mutations in these genes, and eventually to their complete loss, leaving only those genes that are required for the relatively-stable life-style and for maintenance of the symbiosis. Furthering these studies, this work includes a comprehensive study of protein length evolution in obligate insect endosymbionts compared to their free-living relatives, ii testing the long-held assumption that size reductions in individual genes due to small- scale deletions have impacted genome reduction. This was tested using orthologous protein sets from the Flavobacteriaceae (phylum: Bacteroidetes) and Enterobacteriaceae (subphylum: Gammaproteobacteria) families, each of which includes some of the smallest known genomes. Upon examination of protein lengths, we found that proteins were not uniformly shrinking with genome reduction, but instead increased in length variability. Additionally, as complete gene loss also contributes to overall genome shrinkage, we found that the largest proteins in the proteomes of non-host-restricted bacteroidetial and gammaproteobacterial species often were inferred to be involved in secondary metabolic processes, extracellular sensing, or of unknown function. These proteins were absent in the proteomes of obligate insect endosymbionts. Therefore, loss of large proteins not required for host-restricted lifestyles in obligate endosymbiont proteomes likely contributes to extreme genome reduction to a greater degree than protein shrinkage. To further test these conserved patterns of genome evolution in insect mutualists and to gain insight into a newly described insect-bacterial symbiosis, we sequenced the complete genome of the obligate bacterial symbiont of Halyomorpha halys, an invasive pest of the US. Many phytophagous stink bugs, including H. halys, harbor gammaproteobacterial symbionts necessary for host development. "Candidatus Pantoea carbekii" is the primary occupant of gastric caeca lumina flanking the distal midgut of H. halys insects and is vertically transmitted. To infer contributions of “Ca. P. carbekii" to H. halys, the complete genome was sequenced and annotated from a North American H. iii halys population. Overall, the “Ca. P. carbekii" chromosome is nearly one-fourth (1.2 Mb) that of free-living congenerics, yet retains genes encoding many functions that are potentially host-supportive, including nutrient provisioning genes, similar to other mutualists of plant-feeding insects. These genomic resources aid in the continued exploration of animal-bacterial mutualisms. iv This document is dedicated to my family and significant other. v Acknowledgments In addition to the helpful anonymous reviewers of the published work presented here, I would like to thank Franklin Sun and Rafah Asadi for developing Java programs and Python scripts, respectively, used in analyses described in Chapter 1. I am extremely grateful the time and effort dedicatd by my vibrant, inspiring, and supportive committee including Andy Michel, Kelly Wrighton, Normon Johnson, and my advisor, Zakee Sabree. Zakee is an outstanding mentor that is constantly excited about science, encourages me to excel in my field, is exceptionally creative, and dedicated to his mentorship. I am proud to have been Zakee’s student and will continue to emulate his intelligence and enthuisam for science. vi Vita 2010................................................................B.S. Zoology, University of Florida 2011 to present ..............................................Graduate Student, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University Publications LJ Kenyon, T Meulia, and ZL Sabree. “Habitat visualization and genomic analysis of "Candidatus Pantoea carbekii", the primary symbiont of the brown marmorated stink bug.” Genome Biology and Evolution (in revision). LJ Kenyon and ZL Sabree. "Obligate insect endosymbionts exhibit increased ortholog length variation and loss of large accessory proteins concurrent with genome shrinkage." Genome Biology and Evolution 6.4 (2014): 763-775. RD Denton, LJ Kenyon, KR Greenwald, and HL Gibbs. "Evolutionary basis of mitonuclear discordance between sister species of mole salamanders (Ambystoma sp.)." Molecular Ecology 23.11 (2014): 2811-2824. F Michonneau, K Netchy, J Starmer, S McPherson, CA Campbell, SG Katz, L Kenyon et al. "Mitochondrial markers reveal many species complexes and non-monophyly vii in aspidochirotid holothurians." Echinoderms in a Changing World: Proceedings of the 13th International Echinoderm Conference, January 5-9 2009, University of Tasmania, Hobart Tasmania, Australia. CRC Press, 2012. Fields of Study Major Field: Evolution, Ecology, and Organismal Biology viii Table of Contents Abstract……………………………………………………………………………………ii Dedication………………………………………………………………………………....v Acknowledgments………………………………………………………………………..vi Vita…………………………………………………………………………………...….vii Publications……………………………………………………………………………...vii Fields of Study………………………………………………………………………..…viii Table of Contents………………………………………………………………………....ix List of Tables……………………………………………………………………………xiv List of Figures………………………………………………………………………...….xv Chapter 1: Obligate insect endosymbionts exhibit increased ortholog length variation and loss of large accessory proteins concurrent with genome shrinkage……………………...1 I. Introduction.…………………………………………………………………….1 II. Methods ………………………………………………………………………..4 A. Selection of taxa used in study ………………………………………...4 B. Detection of orthologous proteins and domain regions.……………….5 C. Calculating gap frequencies in orthologous protein alignments.………6 D. Evaluation of the maximum protein length in Gammaproteobacteria and Bacteroidetes proteomes ……………………………………………..6 III. Results…………………………………………………………………………7 ix A. Orthologous proteins and bacterial lineages used in this study……..…7 B. Obligate insect endosymbiont orthologs exhibit increased protein length variation …………………………………………………...………7 C. Indel mutations at protein terminuses.…………………………..……18 D. Large proteins invovled in secondary cellular processes are absent in OIE proteomes………………………………………………………...18 IV. Discussion……………………………………………………………………21 A. Increased length variability, and not uniform shrinkage, typifies endosymbiont orthologs.…………………………………………………21 B. No sacred ground: functional domains and linker regions of OIE proteins both exhibit elevated length variability.………………………...25 C. Use it or lose it: the loss of genes encoding large, non-essential proteins contributes to genome shrinkage in endosymbiotic lineages.……………27 V. Concluding Remarks.…………………………………………………………30 Chapter 2: Habitat visualization and genomic analysis of "Candidatus Pantoea carbekii", the primary symbiont of the brown marmorated stink bug………………………………32 I. Introduction……………………………………………………………………32 II. Methods…………………………………………………………………….…35 A. Genome sequencing and annotation……………………………….…35 B. Comparative analysis…………………………………………………40 C. Molecular and phylogenetic reconstruction…………………………..41 D. SNP and genomic synteny analysis………………………………..…41 x E. H. halys gut microbiome analysis………………………………….…42 F. Fluorescence in situ hybridization and electron microscopy…………43 G. Protein analysis of egg lavage………………………………………..46 III. Results……………………………………………………………….………47 A. P. carbekii dominates the H. halys crypt-bearing midgut and is abundant on egg surfaces…………….………………………………….47 B. P. carbekii exhibits genome shrinkage and other consequences of host restriction……………………………………………………………..….51 C. P. carbekii metabolism and putative role in H. halys physiology……55 D. P. carbekii plasmids encode genes important for nitrogen assimilation and thiamine biosynthesis……………………………….………………58 E. Degradation of DNA replication and repair mechanisms and abundant SNPs between P. carbekii strains………………………….……….……61 F. Degraded cell division genes may contribute to elongated cell morphology………………………………………………………………64 G. Stress tolerance in
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