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From Bathtubs to Bloodfeeders: an Evolutionary Study of the Alphaproteobacterial Gellertiella (Formerly Ca

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From Bathtubs to Bloodfeeders: an Evolutionary Study of the Alphaproteobacterial Gellertiella (Formerly Ca From bathtubs to bloodfeeders: an evolutionary study of the alphaproteobacterial Gellertiella (formerly Ca. Reichenowia) by Kevin C. Anderson A thesis submitted in conformity with the requirements for the degree of Master's of Science Graduate Department of Ecology & Evolutionary Biology University of Toronto © Copyright 2021 by Kevin C. Anderson Abstract From bathtubs to bloodfeeders: an evolutionary study of the alphaproteobacterial Gellertiella (formerly Ca. Reichenowia) Kevin C. Anderson Master's of Science Graduate Department of Ecology & Evolutionary Biology University of Toronto 2021 Many leeches are blood feeders and host bacteria within specialized organs. One example is Placobdella which hosts the α-proteobacterial Candidatus Reichenowia. It is assumed that Reichenowia provisions Placobdella with B vitamins. Although Reichenowia consistently places within Rhizobiaceae, its free-living relative remains a mystery. By obtaining genome sequences of the endosymbiotic bacteria of six species of Placobdella, I address questions regarding the role of Reichenowia and its origin. B vitamin synthesis pathways remain largely intact across all taxa with many gaps likely representing a lack of knowledge concerning alternate synthesis routes. I find robust and consistent support for the nesting of the free-living Gellertiella hungarica within Reichenowia, necessitating the dissolution of Reichenowia. The topology of this clade suggests two independent origins of endosymbiosis from a G. hungarica-like ancestor. These findings clarify the ecology of the system and point towards a potentially novel model system for investigating the early stages of endosymbiosis. ii To Nana. Acknowledgements Many people were instrumental in the completion of this thesis, both directly and indirectly. First and foremost I owe huge thanks to my superb supervisory team in Sebastian Kvist and Alejandro Manzano-Mar´ın for trusting me to take on this project and guiding me through my research in perhaps one of the strangest years on record. Claire Manglicmot has played a large role in making this thesis topic a possibility and for helping to generate the data which is the basis of the study presented within. My supervisory committee, composed of Megan Frederickson and Rob Ness, is also to thank for the helpful input and suggestions which greatly improved the quality of the research. The entirety of the Kvist Lab (as well as some of its recent graduates), helped not only in the betterment of my research but also were (and continue to be) dearly cherished friends; thank you to Danielle de Carle, Rafael Eiji Iwama, Maddy Foote, Claire Manglicmot, Ismay Earl, and Sophia Fan. For assistance funding this research I acknowledge, and am grateful for, the support of the Natural Sciences and Engineering Research Council of Canada (NSERC). I also wish to thank Mrs. Ellen B. Freeman for her contributions to the Reino S. Freeman graduate scholarship and for enabling research that I hope will honour the legacy of her husband. Lastly, and certainly not leastly, I wish to thank my family and friends for providing a source of support and comfort that I would not be here without. Chief among these are Georgia Harrison, Jennifer Potvin, Christopher Anderson, and Jacob Taylor. This list is not extensive (how could it be?) so to all those listed and unlisted, thank you again, for everything. iii Contents Acknowledgements............................................. iii List of Tables................................................v List of Figures............................................... vi 1 Reichenowia 1 1.1 Introduction..............................................1 1.2 Materials & Methods.........................................3 1.2.1 Specimen Collection.....................................3 1.2.2 Genome Sequencing & Assembly..............................4 1.2.3 Metabolic Reconstruction..................................4 1.2.4 Phylogenomic Analyses...................................6 1.2.5 Similarity analyses......................................7 1.3 Results.................................................7 1.3.1 Genome characteristics of Gellertiella and Reichenowia.................7 1.3.2 Similarity analyses......................................8 1.3.3 Phylogenomic placement of Reichenowia.......................... 10 1.3.4 B-vitamin synthesis capabilities............................... 13 1.4 Discussion............................................... 16 1.4.1 Taxonomic status of Candidatus Reichenowia....................... 16 1.4.2 The functional role of endosymbiotic Gellertiella ..................... 16 1.4.3 Phylogenomic placement of Gellertiella .......................... 18 1.4.4 The origin of endosymbiosis in Gellertiella ......................... 18 1.4.5 Outstanding questions and future directions........................ 20 Bibliography 31 Appendices 32 A Supplementary material 32 iv List of Tables 1.1 Leech and symbiont sampling localities and accession numbers.................5 1.2 Genome characteristics of Reichenowia and Gellertiella hungarica ................8 1.3 ANI and 16S identity similarity matrix...............................8 A.1 Metadata for taxa used during the genome assembly process................... 33 A.2 Taxonomic information for each of the taxa used during the metabolic reconstruction..... 33 A.3 Metadata for each B vitamin pathway reconstructed....................... 34 A.4 Metadata for the taxa used for the phylogenomic reconstructions................ 37 A.5 Topology test results......................................... 37 v List of Figures 1.1 Ecological data for putative G. hungarica and Reichenowia sequences retreived from the NCBI sequence read archive........................................9 1.2 Ribosomal phylogeny of select Rhizobiales............................. 11 1.2 Ribosomal phylogeny of select Rhizobiales (continued)...................... 12 1.3 An overview of the B vitamin metabolism of Gellertiella hungarica and Reichenowia spp... 14 A.1 Ribosomal, amino acid coded, partitioned, Bayesian tree..................... 38 A.2 Ribosomal, amino acid coded, unpartitioned, maximum likelihood tree............. 39 A.3 Ribosomal, amino acid coded, unpartitioned, Bayesian tree................... 40 A.4 Ribosomal, nucleotide coded, partitioned, maximum likelihood tree............... 41 A.5 Ribosomal, nucleotide coded, unpartitioned, maximum likelihood tree............. 42 A.6 Orthologue, amino acid coded, unpartitioned, maximum likelihood tree............ 43 A.7 An overview of the B vitamin metabolism of Gellertiella hungarica ............... 44 A.8 An overview of the B vitamin metabolism of Reichenowia sp. strain Ppha........... 45 A.9 An overview of the B vitamin metabolism of Reichenowia sp. strain Pmon........... 46 A.10 An overview of the B vitamin metabolism of Reichenowia sp. strain Pmul........... 47 A.11 An overview of the B vitamin metabolism of Reichenowia sp. strain Ppar........... 48 A.12 An overview of the B vitamin metabolism of Reichenowia sp. strain Prug........... 49 A.13 An overview of the B vitamin metabolism of Reichenowia sp. strain Psp............ 50 vi Chapter 1 Reichenowia 1.1 Introduction Endosymbiosis is a widespread, evolutionarily convergent, phenomenon amongst both prokaryotes and eu- karyotes [1,2] wherein, most commonly, a prokaryotic taxon becomes intimately ( i.e., intracellularly) asso- ciated with a eukaryotic host. Different endosymbionts have varied roles within their hosts depending upon the host's specific needs (e.g. [3{5]). One such role is nutrient provisioning - when a highly specialized host diet (e.g. phloem feeding) lacks essential nutrients that the host cannot synthesize [6]. In these cases, it is common for the host-associated endosymbiont to retain the genetic repertoire neccessary for the synthesis of these nutrients. Although experiments that correlate symbiont removal and ad hoc nutrient exposure with host fitness and/or survival remain the gold-standard for determining the functional basis of a symbiosis (e.g.,[7]), the recent advances in our ability to cheaply and accurately sequence genomes with even small samples of tissue have made the inference of an endosymbiont's function possible from a genome sequence alone. However, our power to make a functional prediction regarding the role of an endosymbiont based on a genome sequence would be considerably weakened without the extremely derived features that have been observed among the genomes of (especially) obligate, vertically transmitted endosymbionts. Briefly, these consist of a (generally) drastic reduction in the size of the endosymbiont genome compared to its free-living relative, an unusually high AT bias in terms of the genome's base composition, an increased rate in sequence evolution (again compared to a free-living relative), and even a reduction in the ability to translate mRNA in an optimal fashion [2,6,8{10]. These genomic features are thought to have arisen as a byproduct of mostly non-adaptive processes: specifically, the clock-like population bottlenecks and lack of recombination between populations of vertically transmitted, obligate endosymbionts results in the total relaxation of selection on `non-essential' elements of the genome and reduces the power of selection to maintain even those elements that are crucial for the proper functioning of the endosymbiosis. However, the rather binary overview pro- vided above fails to account for important elements such as the relative importance of the endosymbiont (i.e.,
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