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Mitchell, C. E.

Publications and source records attributed to Mitchell, C. E..

10 recordsLinked to original sources

Environment and host infection history jointly predict disease risk in a multi-pathogen system

Forecasting disease epidemics may require considering both abiotic and biotic conditions. Abiotic conditions can influence pathogen dispersal, survival, and infection, while prior infection by one pathogen species can alter host susceptibility to subsequent pathogens, creating historical contingencies. Yet, the relative importance of environmental conditions, within-host pathogen interactions, and their interplay in predicting seasonal disease dynamics remains underexplored. We analyzed approximately 30,000 plant-level observations of three foliar fungal diseases on the grass species tall fescue in a North Carolina old field, and meteorological data, from 2017-2024. Using such datasets to make ecological predictions that are accurate and interpretable may require multiple modeling approaches. Temporally explicit random forest models predicted future disease with over 80% accuracy for two of the three diseases and revealed environmental thresholds for disease prediction in environmental variables including temperature and humidity. Survival analyses showed that pathogen-pathogen interactions rivaled environmental conditions in predicting risk of crown rust, which was strongly facilitated by prior anthracnose infection. Across all pathogens, Bayesian hierarchical models recovered evidence that facilitative interactions between coinfecting pathogens were modulated by effects of environmental conditions, particularly temperature. Together, these complementary approaches show that a host's current disease state can matter as much as its environment in predicting disease, identify key environmental factors associated with disease risk, and show that modulation of environmental drivers by pathogen coinfections can improve predictions of seasonal disease epidemics. Other disease forecasts may be improved by accounting not just for environmental drivers, but also how those drivers propagate through pathogen species interactions.

ecology↗

A Fkh1/2 binding site array in the WHI5 promoter drives sub-scaling transcription

Cells typically regulate their size within a relatively tight range by coupling growth to the cell division cycle using a dedicated set of molecular mechanisms. In budding yeast, cells are born with a similar amount of the G1/S inhibitor protein Whi5 that is then diluted by growth throughout G1. As cells grow, Whi5 concentration decreases and cells become more likely to enter the cell cycle. Cells are born in G1 with similar amounts of Whi5 because of the size-independent (sub-scaling) expression of WHI5 mRNA during S/G2/M phases and the equal partitioning of Whi5 protein at division. While the latter is known to be achieved by association with chromatin before anaphase, the mechanism for the former is poorly understood. Through systematic mutations of the WHI5 promoter, we discovered that WHI5s core promoter region located -126 to -75 base pairs upstream of the start codon is responsible for sub-scaling expression. This sequence contains a repeating array of binding sites for the transcription factors Fkh1 and Fkh2. Mutation of any of these sites, deletion of either FKH1 or FKH2, or preventing Fkh1 or Fkh2 dimerization weakens the sub-scaling of WHI5 transcription. Taken together with structural predictions and a mathematical model of cooperative Fkh-DNA binding, we conclude that WHI5s sub-scaling transcription is regulated by a Fkh1/2 heteropolymer binding an array of sites in its core promoter.

cell biology↗

Amplification of disease by nutrient addition: Testing mechanisms from individual to community levels

Nutrient supply can amplify disease epidemics through mechanisms from individual to community levels. Within host individuals, nutrient addition can drive pathogen replication or growth. Across a host population, nutrient addition can drive disease transmission by increasing host growth and abundance relative to defense. Furthermore, such effects may be influenced by pathogen species interactions. Understanding how nutrients impact disease epidemics requires a framework that integrates these mechanisms across biological levels. To build such a framework, we conducted a field experiment in an old field on tall fescue, Lolium arundinaceum, and used structural equation models to integrate multiple hypothesized mechanisms. Nutrient addition (NPK fertilizer) increased brown patch disease but was best modeled as a direct path and not mediated by host abundance. To expand our framework, we also re-analyzed a previous experiment. That experiment reproduced the direct path from nutrients to disease, and added an indirect path mediated by host population abundance. Nutrient addition also increased foliar nitrogen, consistent with individual-level mechanism, but this did not increase disease. Brown patch decreased with burden of another disease, anthracnose, independently of nutrients. These results partially support both individual- and population-level hypotheses, emphasizing the importance of considering multiple biological levels underlying impacts of abiotic change.

ecology↗

Order of arrival and nutrient supply alter outcomes of coinfection with two fungal pathogens

A pathogen arriving on a host typically encounters a diverse community of microbes that can shape priority effects, other within-host interactions, and infection outcomes. In plants, environmental nutrients can drive tradeoffs between host growth and defense and can mediate interactions between coinfecting pathogens. Nutrients may thus alter the outcome of pathogen priority effects for the host, but this possibility has received little experimental investigation. To disentangle the relationship between nutrient availability and coinfection dynamics, we factorially manipulated nutrient availability and order of arrival of two foliar fungal pathogens (Rhizoctonia solani and Colletotrichum cereale) on the host grass tall fescue (Festuca arundinacea) and tracked disease outcomes. Overall, C. cereale infection facilitated infection by R. solani, increasing its infection rate regardless of their order of inoculation. Additionally, simultaneous and C. cereale-first inoculations decreased plant growth and - in plants that did not receive nutrient addition - increased leaf nitrogen concentrations compared to uninoculated plants. Nutrient addition did not influence infection rates, severity of infection, or plant biomass. These findings highlight the importance of understanding the intricate associations between the order of pathogen arrival, host nutrient availability, and host defense to better predict infection outcomes.

ecology↗

Disease decreases variation in host community structure in an old-field grassland

Disease may modulate variation in host community structure by modifying the interplay of deterministic and stochastic processes. For instance, deterministic processes like ecological selection can benefit species less impacted by disease. When disease consistently selects for certain host species, this can reduce variation in host community composition. On the other hand, when host communities are less impacted by disease and selection is weaker, stochastic processes (e.g., drift, dispersal) may play a bigger role in host community structure, which can increase variation in structure among communities. While effects of disease on host community structure have been quantified in field experiments, few have addressed the role of disease in modulating variation in structure among host communities. To address this, we conducted a field experiment spanning three years, using a tractable system: foliar fungal pathogens in an old-field grassland community dominated by the grass Lolium arundinaceum, tall fescue. We reduced foliar fungal disease burden in replicate host communities (experimental plots in intact vegetation) in three fungicide regimens that varied in the duration of fungicide exposure and included a fungicide-free control. We measured host diversity, biomass, and variation in community structure among replicate communities. Disease reduction generally decreased plant richness and increased aboveground biomass relative to communities experiencing ambient levels of disease. Despite changes in structure of the plant communities over the experiments three years, the effects of disease reduction on plant richness and biomass were consistent across years. However, disease reduction did not reduce variation in host community structure, providing little evidence for ecological selection by competition or other deterministic processes. Instead, disease reduction tended to amplify variation in host community structure among replicate communities (i.e., within fungicide treatment groups), suggesting that disease diminished the degree to which host communities were structured by stochastic processes. These results of experimental disease reduction both highlight the potential importance of stochastic processes in plant communities and reveal the potential for disease to regulate variation in host community structure.

ecology↗

A microbial mutualist within host individuals increases parasite transmission between host individuals: Evidence from a field mesocosm experiment

The interactions among host-associated microbes and parasites can have clear consequences for disease susceptibility and progression within host individuals. Yet, empirical evidence for how these interactions impact parasite transmission between host individuals remains scarce. We address this scarcity by using a field mesocosm experiment to investigate the interaction between a systemic fungal endophyte, Epichloe coenophiala, and a fungal parasite, Rhizoctonia solani, in leaves of a grass host, tall fescue. Specifically, we investigated how this interaction impacted parasite transmission under field conditions in replicated experimental host populations. Epichloe-inoculated populations tended to have greater disease prevalence over time, though this difference had weak statistical support. More clearly, Epichloe-inoculated populations experienced higher peak parasite prevalences than Epichloe-free populations. Epichloe conferred a benefit in growth; Epichloe-inoculated populations had greater aboveground biomass than Epichloe-free populations. Using biomass as a proxy, host density was correlated with peak parasite prevalence, but Epichloe still increased peak parasite prevalence after controlling for the effect of biomass. Together, these results suggest that within-host microbial interactions can impact disease at the population level. Further, while Epichloe is clearly a mutualist of tall fescue, it may not be a defensive mutualist in relation to R. solani.

ecology↗

Host exposure to symbionts and ecological drift generate divergence in parasite community assembly

The initial colonization of a host by symbionts, ranging from parasites to mutualists, can generate priority effects that alter within-host interactions and the trajectory of parasite community assembly. At the same time, variation in parasite communities among hosts can also stem from stochastic processes. Community ecology theory posits that multiple processes (e.g. dispersal, selection and drift) interact to generate variation in community structure, but these processes are rarely considered simultaneously during community assembly. To test the role of these processes in a parasite community, we experimentally simulated dispersal of three symbionts by factorially inoculating individual plants of tall fescue with two foliar fungal parasites, Colletotrichum cereale and Rhizoctonia solani, and a hypothesized mutualist endophyte, Epichloe coenophiala. We then tracked parasite infections longitudinally in the field. After the initial inoculations, hosts were exposed to a common pool of parasites in the field, which we expected to cause parasite communities to converge towards a similar community state. To test for convergence, we analyzed individual hosts parasite community trajectories in multivariate space. In contrast to our expectation, there was no signal of convergence. Instead, parasite community trajectories generally diverged over time between treatment groups and the magnitude of divergence depended on the symbiont species inoculated. Parasite communities of hosts that were inoculated with only the mutualist, Epichloe, showed significant trends of divergence relative to all other symbiont inoculation treatments. In contrast, hosts inoculated with only Rhizoctonia did not exhibit clear trends of divergence when compared to other parasite inoculations. Further, co-inoculation with both parasite species resulted in faster rates of divergence and greater temporal change in parasite communities relative to hosts inoculated with only the parasite Colletotrichum. As predicted by existing theory, parasite communities showed evidence of drift during the beginning of the experiment, which contributed to among-host divergence in parasite community structure. Overall, these data provide evidence that initial dispersal of symbionts produced persistent changes in parasite community structure via ecological selection, that drift was important during the early stages of parasite community assembly, and together, dispersal, selection and drift resulted in parasite community divergence. Open Research statementThe data and code that support the findings of this study are available through Zenodo at https://doi.org/10.5281/zenodo.5714452

ecology↗

Higher-order interactions among coinfecting parasites and a microbial mutualist impact disease progression

Interactions among parasites and other microbes within hosts can impact disease progression, yet study of such interactions has been mostly limited to pairwise combinations of microbes. Given the diversity of microbes within hosts, higher-order interactions among more than two microbial species may also impact disease. To test this hypothesis, we performed inoculation experiments that investigated interactions among two fungal parasites, Rhizoctonia solani and Colletotrichum cereale, and a systemic fungal endophyte, Epichloe coenophiala, within a grass host. Both pairwise and higher-order interactions impacted disease progression. While the endophyte did not directly influence R. solani growth or C. cereale symptom development, the endophyte modified the interaction between the two parasites. The magnitude of the facilitative effect of C. cereale on the growth of R. solani tended to be greater when the endophyte was present. Moreover, this interaction modification strongly affected leaf mortality. For plants lacking the endophyte, parasite co-inoculation did not increase leaf mortality compared to single-parasite inoculations. In contrast, for endophyte-infected plants, parasite co-inoculation increased leaf mortality compared to inoculation with R. solani or C. cereale alone by 1.9 or 4.9 times, respectively. Together, these results show that disease progression can be strongly impacted by higher-order interactions among microbial symbionts.

ecology↗

Parasites as niche modifiers for the microbiome: A field test with multiple parasites

Parasites can affect and be affected by the hosts microbiome, with consequences for host susceptibility, parasite transmission, and host and parasite fitness. Yet, there are two aspects of the relationship between parasite infection and the host microbiome that remain little understood: the nature of the relationship under field conditions, and how the relationship varies among parasite species. To overcome these limitations, we assayed the within-leaf fungal community in a grass population to investigate how diversity and composition of the fungal microbiome are associated with natural infection by fungal parasites with different feeding strategies. We hypothesized that parasites that more strongly modify niches available within a host will thereby alter the microbial taxa that can colonize the community and be associated with greater changes in microbiome diversity and composition. A parasite that creates necrotic tissue to extract resources (necrotrophs) may act as a particularly strong niche modifier whereas one that does not (biotrophs) may not. Barcoded amplicon sequencing of the fungal ITS region revealed that the microbiome of leaf segments that were symptomatic of necrotrophs had lower fungal diversity and distinct composition compared to segments that were asymptomatic or symptomatic of other parasites. There were no clear differences in fungal diversity or composition between leaf segments that were asymptomatic and segments that were symptomatic of other parasite feeding strategies. This supports the hypothesis that within-host niches link infection by parasites to the hosts microbiome. Together, these results highlight the importance of parasite traits in determining parasite impacts on the hosts microbiome.

ecology↗

Host community assembly modifies the relationship between host and parasite richness

Host and parasite richness are generally positively correlated, but the stability of this relationship during community assembly remains untested. The composition of host communities can alter parasite transmission, and the relationship between host and parasite richness is sensitive to parasite transmission. Thus, changes in composition during host community assembly could strengthen or weaken the relationship between host and parasite richness. Host community assembly, in turn, can be driven by many processes, including resource enrichment. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness, we experimentally crossed host diversity and resource supply to hosts, then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post-assembly host species richness, richness-independent host phylogenetic diversity, and colonization by exotic host species. Throughout community assembly, host richness predicted parasite richness. As predicted, this effect was moderated by exotic abundance: communities dominated by exotic species exhibited a stronger positive relationship between post-assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness, providing a novel mechanism to explain contingencies in this relationship.

ecology↗