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Characteristics of genome evolution in obligate insect symbionts, including the description of a recently identified obligate extracellular symbiont.

Kenyon, Laura J
http://rave.ohiolink.edu/etdc/view?acc_num=osu1418408362

Abstract Details

2015, Master of Science, Ohio State University, Evolution, Ecology and Organismal Biology.
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, 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. 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.
Zakee Sabree (Advisor)
Kelly Wrighton (Committee Member)
Andrew Michel (Committee Member)
Norman Johnson (Committee Member)
161 p.
Biology; Evolution and Development; Microbiology

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Citations

  • Kenyon, L. J. (2015). Characteristics of genome evolution in obligate insect symbionts, including the description of a recently identified obligate extracellular symbiont. [Master's thesis, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1418408362

    APA Style (7th edition)

  • Kenyon, Laura. Characteristics of genome evolution in obligate insect symbionts, including the description of a recently identified obligate extracellular symbiont. 2015. Ohio State University, Master's thesis. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1418408362.

    MLA Style (8th edition)

  • Kenyon, Laura. "Characteristics of genome evolution in obligate insect symbionts, including the description of a recently identified obligate extracellular symbiont." Master's thesis, Ohio State University, 2015. http://rave.ohiolink.edu/etdc/view?acc_num=osu1418408362

    Chicago Manual of Style (17th edition)

osu1418408362
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