Defense Date
6-11-2024
Graduation Date
Summer 6-11-2024
Availability
Immediate Access
Submission Type
dissertation
Degree Name
PhD
Department
Biological Sciences
School
School of Science and Engineering
Committee Chair
Sarah Woodley
Committee Member
Wook Kim
Committee Member
Jan Janecka
Committee Member
Kevin Kohl
Keywords
Microbiota, Microbiota-Gut-Brain, Frog, Tadpole. Brain, Behavior, Neurodevelopment, Physiology
Abstract
Microbial communities comprising bacteria, viruses, fungi, and protists live within and on the surfaces of animal hosts. These microbial communities exist in symbiosis with the host, and heavily influence host physiology, development, health, and fitness. Gut-dwelling microbes (i.e., gut microbiota) contribute to host neurodevelopment through a bidirectional Microbiota-Gut-Brain (MGB) axis. Evidence of the MGB axis has been primarily derived from studies that use germ-free (GF) models, which commonly display altered neurophysiology and behavior compared to conventionally raised counterparts. Almost all studies of the MGB axis have used mammalian models in a biomedical framework, leaving a knowledge gap regarding the role of the gut microbiota in neurodevelopment and behavior in non-mammalian animals and in more ecological contexts. The goal of my dissertation was to evaluate how the aquatic microbial environment influences the biodiversity of the amphibian gut microbiota, and how these shifts in the microbiota influence amphibian neurodevelopment and behavior. Findings of associations between the gut microbiota and amphibian neurodevelopment and behavior are consistent with the presence of a MGB axis and can offer insight as to whether particular aspects of the gut microbiota (i.e., diversity and taxa abundance) were significantly associated with tadpole development and physiology. First, I tested whether manipulation of the gut microbiota affected the brain development of Green Frog (Lithobates clamitans) tadpoles. Tadpoles were raised in natural (unmanipulated) pond water or autoclaved pond water at three different water temperatures: 14, 22 and 28°C. Autoclaving reduced the number of aquatic microbes available to colonize the tadpole and thereby resulted in a gut microbiota with reduced microbial biodiversity and altered community composition compared to tadpoles raised in natural pond water. Both temperature and the aquatic microbial community during development affected tadpole brain shape, and the biodiversity of the tadpole gut microbiota was negatively associated with the size of the optic tectum. These results provide some of the first evidence of the MGB axis in amphibians. Next, I examined an additional species and incorporated behavioral assays to evaluate potential functional consequences of gut microbial manipulation. To do this, I raised Northern Leopard Frog (Lithobates pipiens) tadpoles in natural or autoclaved pond water. Compared to tadpoles raised in natural pond water, tadpoles raised in autoclaved pond water: (1) had altered gut microbial community composition and decreased biodiversity, (2) had decreased locomotory responses to visual stimuli, (3) had relatively heavier brains and altered brain shape, and (4) were larger and developed faster. Additionally, the composition and diversity of the gut microbiota was a significant predictor of tadpole brain size, brain shape, and locomotory behavior. Finally, I tested whether exposure to both a depleted aquatic microbial community and an ecological stressor had interactive effects on physiological and neurodevelopmental endpoints in tadpoles. In mammals, the composition of the gut microbiota, and subsequently the development of the MGB axis, is shaped by stressors. Due to frequent exposure of wildlife to relevant ecological stressors such as predation, examining the role of stressors on the formation of the gut microbiota and subsequent physiological and neurodevelopmental endpoints is of interest. I exposed tadpoles to predation-derived chemical cues, exogenous corticosterone (CORT), or a vehicle control. I simultaneously exposed tadpoles to either natural or autoclaved pond water. I found no clear effects of predator cues, but tadpoles exposed to CORT had altered composition of their gut microbiota, altered brain shape, and altered tail shape compared to control. Additionally, I replicated previous results by finding that tadpoles raised in autoclaved pond water were larger, had altered brain development, and a dramatically altered gut microbiota that predicted several neurodevelopmental endpoints. Encouragingly, tadpoles raised in autoclaved pond water also displayed reduced ability to evade predators, which likely impacts fitness and survival. I found surprisingly few interactive effects of the aquatic microbial community and stressors. Overall, my dissertation work provides novel evidence of the MGB axis in larval amphibians. My work highlights the importance of the promotion and maintenance of freshwater ecosystem health, as aquatic microbial communities present in these waters are shown to have dramatic and consistent impacts on amphibian body size, neurodevelopment, and fitness-related behaviors.
Language
English
Recommended Citation
Emerson, K. (2024). The Aquatic Microbial Environment Shapes the Gut Microbiota, Brain, and Behavior of Larval Amphibians (Doctoral dissertation, Duquesne University). Retrieved from https://dsc.duq.edu/etd/2237
Additional Citations
Emerson, K. J., Fontaine, S. S., Kohl, K. D. and Woodley, S. K. (2023). Temperature and the microbial environment alter brain morphology in a larval amphibian. Journal of Experimental Biology 226.
Emerson, K. J. and Woodley, S. K. (2024). Something in the water: aquatic microbial communities influence the larval amphibian gut microbiota, neurodevelopment and behaviour. Proceedings of the Royal Society B 291, 20232850.