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Population dynamics of Vibrio cholerae and its close relative Vibrio metoecus in an aquatic ecosystem Open Access


Other title
Vibrio cholerae
Population Dynamics
Type VI Secretion System
Type of item
Degree grantor
University of Alberta
Author or creator
Kirchberger, Paul C.
Supervisor and department
Boucher, Yan
Examining committee member and department
Buckley, Daniel (Soil and Crop Sciences Cornell)
Gallin, Warren (Biological Sciences)
Hazes, Bart (Medical Microbiology & Immunology)
Lanoil, Brian (Biological Sciences)
Department of Biological Sciences
Microbiology and Biotechnology
Date accepted
Graduation date
2017-11:Fall 2017
Doctor of Philosophy
Degree level
Vibrio cholerae, because of its role as the causative agent of cholera pandemics, is an extraordinarily well studied microorganism. Decades of research have uncovered a plethora of molecular mechanisms and a wealth of genomic information related to the organisms’ lifestyle as a pathogen. V. cholerae is also easily kept in a laboratory setting and, as a common member of bacterial communities in brackish waters and coastal areas worldwide, is readily isolated in large numbers. These two properties make it an ideal organism to study the population dynamics and evolution of aquatic bacteria. However, decades of pathogenicity-focused research have left us with little understanding of even the baseline structure of a natural population of V. cholerae. Importantly, the ecology of numerous non-pathogenic lineages of this organism is largely unknown. In this thesis, I aim to test the hypothesis that various lineages of V. cholerae have evolved to occupy a number of different ecological niches, and develop a baseline understanding of the population structure and dynamics of this species. By combining multi-locus sequence typing of over 400 Vibrio isolates and whole genome sequencing of selected strains from a pond ecosystem in the eastern United States, I discovered a highly clonal population structure dominated by only a few, phylogenetically distinct lineages. A larger number of non-dominant lineages exist in low abundance and undergo strong fluctuations in the span of a month. I also classify a particularly divergent lineage of V. cholerae as a new, phylogenetically and phenotypically distinct species, V. metoecus. This species represents the closest discovered relative to V. cholerae to date and is an example of recent ecological niche separation. Among a number of potentially ecologically relevant genes differentiating lineages of V. cholerae, I discovered an extraordinary diversity of Type VI secretion system (T6SS) associated effector and immunity genes. Based on evidence from extant genomes, I describe a mechanism of horizontal gene transfer and illegitimate recombination that leads to the evolution of complex arrays of effector and immunity genes unique to each lineage of V. cholerae and V. metoecus at our sampling site. Finally, I develop a high-throughput sequencing method for a variable region of a gene exclusive to V. cholerae that allows the culture-independent study of its population structure at unprecedented scale. In addition to confirming the results of my isolation-based study, I uncover drastic shifts in the population structure of V. cholerae over the course of two years, including the invasion of a non-endemic strain after a seasonal depletion of the local Vibrio population. Furthermore, I demonstrate pervasive mosaic sympatry, with sampling sites 5m apart harbouring different strains of V. cholerae, perhaps mediated by their unique T6SS effector-immunity gene combination. Importantly, I also detect the presence of pandemic-related V. cholerae as a minor contributor to this population, sporadically rising to larger relative abundance. I provide evidence that this particular lineage is adapted to life on marine particles, while most V. cholerae lineages are generalists found free-swimming and particle associated. These results, taken together, imply that a mixture of mosaic sympatry and T6SS mediated interactions facilitate the coexistence of multiple lineages of V. cholerae in a single location. Some of these lineages show strong indication of niche-separation, yet a combination of intrinsic and extrinsic factors likely allows members of the species to diverge significantly while remaining roughly ecologically equivalent.
This thesis is made available by the University of Alberta Libraries with permission of the copyright owner solely for the purpose of private, scholarly or scientific research. This thesis, or any portion thereof, may not otherwise be copied or reproduced without the written consent of the copyright owner, except to the extent permitted by Canadian copyright law.
Citation for previous publication
Kirchberger PC, Orata FD, Barlow EJ, Kauffman KM, Case RJ, Polz MF, Boucher Y. 2016. A Small Number of Phylogenetically Distinct Clonal Complexes Dominate a Coastal Vibrio cholerae Population. Appl Environ Microbiol 82:5576-5586.Kirchberger PC, Turnsek M, Hunt DE, Haley BJ, Colwell RR, Polz MF, Tarr CL, Boucher Y. 2014. Vibrio metoecus sp. nov., a close relative of Vibrio cholerae isolated from coastal brackish ponds and clinical specimens. Int J Syst Evol Microbiol 64:3208-3214.Kirchberger PC, Unterweger D, Provenzano D, Pukatzki S, Boucher Y. 2017. Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae. Scientific Reports 7:45133.Orata FD, Kirchberger PC, Méheust R, Barlow EJ, Tarr CL, Boucher Y. 2015. The Dynamics of Genetic Interactions between Vibrio metoecus and Vibrio cholerae, Two Close Relatives Co-Occurring in the Environment. Genome biology and evolution 7:2941-2954.Labbate M, Orata FD, Petty NK, Jayatilleke ND, King W, Kirchberger PC, Allen C, Mann G, Mutreja A, Thomson NR, Boucher Y, Charles IG. 2016. A genomic island in Vibrio cholerae with VPI-1 site-specific recombination characteristics contains CRISPR-Cas and type VI secretion modules. Scientific Reports 6.

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