Slowik, Anna Ruth (2023) Ecological considerations of thermal and nutritional interactions in Metarhizium host range evolution: A multidimensional analysis of niche width in insect-pathogenic fungi. PhD thesis, University of Leeds.
Abstract
Host-pathogen interactions are fundamental to the ecological and evolutionary processes in ecosystems, influencing community dynamics, species distribution, and the evolutionary trajectories of both hosts and pathogens. Such interactions are often dictated by coevolutionary forces that drive pathogens to exhibit specialized host-specific adaptations or generalist strategies encompassing multiple hosts. Entomopathogenic fungi (EPF) serve as key models for studying these interactions, exemplifying different degrees of niche specialization - the extent to which an organism is adapted to specific ecological parameters such as host or environmental conditions - in their ecological functionality. This thesis integrates thermal and nutritional ecology to provide a multidimensional analysis of the environmental niche breadth and host range in Metarhizium species, employing experimental and quantitative methods to deepen insights into the ecological dynamics of EPF. The introductory chapter reviews current knowledge on the interactions between EPF and their thermal and nutritional environments, focusing on how these interactions influence host range specifically in the genus Metarhizium. In Chapter 2, the objective was to develop a rapid, high-throughput method for measuring fungal growth in liquid media cultures using microplates and microspectrophotometry. This method, compared and validated against traditional approaches, enhances the precision and speed in assessing growth patterns among various Metarhizium isolates, and offers a high throughput technique for multidimensional niche quantification. Chapter 3 aimed to quantify the nutritional niches of a specialist and a generalist EPF and determine whether host range correlates with nutritional niche width. It was hypothesized that the nutritional niche width of specialist EPF would be narrower, reflecting their ecological lifestyles. Employing the growth assay from Chapter 2 in conjunction with the Geometric Framework for Nutrition, which generates nutritional landscapes by mapping the effects of various nutrient combinations as response topologies, nutrient profiles were produced for the specialist Metarhizium acridum and the more-generalized Metarhizium guizhouense. This approach revealed distinct growth patterns in response to different nutrient availabilities for each fungus. Metarhizium acridum demonstrated greater efficiency in nutrient utilization, growing more overall across various conditions, and protein was more of a limiting factor for M. acridum at lower concentrations compared to M. guizhouense. These findings align with M. acridum’s ecological role as a specialist pathogen that rapidly infects and proliferates in large protein-rich insect populations. Metarhizium guizhouense had a broader nutritional niche and was less sensitive to protein limitation, which reflects its association with carbohydrate-rich plant roots. These findings suggest a relationship between the nutritional niche breadth of these EPFs and their ecological host niches. The final data chapter explores thermal ecology, assessing the influence of thermal adaptation on host-pathogen interactions using EPF with different host ranges and the yellow meal worm, Tenebrio molitor. Central to this study was the Thermal Mismatch Hypothesis (TMH), which proposes that in host-pathogen interactions there is often a mismatch between the optimal temperatures for the growth and virulence of the pathogen and the optimal temperature for the host's immune response or survival. Experiments conducted across ecologically relevant temperatures aimed to construct thermal performance curves for growth and virulence and identify critical thresholds for these traits. It was found that both EPF species and the host shared a growth optima at 28°C, with the host's growth response to infection mediated by the species of fungus and temperature during sublethal infections. However, M. brunneum, the generalist EPF, displayed a broader optimal temperature range for virulence (23-28°C) compared to M. flavoviride, the specialist EPF, which had a multiphasic virulence pattern peaking at 18 and 28°C. Contrary to TMH predictions, peak virulence of both fungi occurred at the host's optimal temperature. Furthermore, the thermal growth profile of M. flavoviride closely matched its temperature-dependent virulence profile, whereas M. brunneum's virulence did not align with its growth across temperatures, indicating that the generalist pathogen may achieve higher virulence even under constrained growth conditions. This investigation uncovers distinct relationships between virulence thermal profiles and individual thermal profiles for Metarhizium brunneum and M. flavoviride, corresponding to their respective evolutionary histories and ecological adaptations. In Chapter 5, I discuss how the cumulative insights into the interactions between abiotic factors and host-pathogen dynamics in these experimental chapters, particularly in Metarhizium species with varied host ranges, contribute to the fundamental understanding of ecological and evolutionary mechanisms driving host-specialization and environmental adaptation in entomopathogenic fungi. In combination with a general review of the current knowledge of the relationship between thermal and nutritional ecology and host specificity in the fungal genus Metarhizium, this thesis presents an integrated approach to understanding the multifaceted adaptations and specializations of Metarhizium species, informing both ecological theory and advancing our knowledge of EPF ecological interactions and roles.
Metadata
Supervisors: | Sait, Steven and De Fine Licht, Henrik and Hesketh, Helen |
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Keywords: | host-pathogen interactions, insect-pathogenic fungi, Metarhizium, Tenebrio molitor, entomopathogenic fungi, nutritional ecology, thermal ecology, niche breadth, ecological specialization, Thermal Mismatch Hypothesis (TMH), virulence profiles, high-throughput growth assay, |
Awarding institution: | University of Leeds |
Academic Units: | The University of Leeds > Faculty of Biological Sciences (Leeds) > School of Biology (Leeds) |
Depositing User: | Mx Anna Ruth Slowik |
Date Deposited: | 08 Apr 2024 13:23 |
Last Modified: | 08 Apr 2024 13:23 |
Open Archives Initiative ID (OAI ID): | oai:etheses.whiterose.ac.uk:34666 |
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