Pathogen-induced Mortality Research Articles

Unravelling a hidden synergy: How pathogen-climate interactions transform habitat hydrology and affect tree growth

Interactions between multiple global change stressors are a defining characteristic of the Anthropocene. Tree-associated pathogens are affecting forested ecosystems worldwide and occur in the context of increased frequency and intensity of extreme climate events such as heat waves, droughts, and floods. The effects of these events, along with subsequent changes in environmental conditions, on remaining and regenerating trees, are not well understood but crucial for the restoration and conservation of forested habitats.In this study, we investigate ash (Fraxinus excelsior) dieback in a temperate broadleaf woodland as a case study to explore the processes influencing non-infected trees during pathogen-induced mortality events. Utilising an experimental setup, we examine tree growth rates at different chronological stages of the disease, including naturally progressing ash dieback (4–5 years since disease outbreak), accelerated ash dieback where ash trees have been girdled (10–15 years), and negligible ash dieback (<20 % ash trees).During a year with typical climatic conditions (2021), soils in accelerated ash dieback plots remained saturated throughout the summer due to insufficient transpiration (57 % higher in the accelerated dieback plots), suggesting a significantly increased risk of summer run-off and floods. However, tree growth rates in these plots were not affected (t-test, t = −0.3 to 1.2, p > 0.05). Conversely, anomalously dry years, such as the 2022 summer drought, saw higher soil moisture in the accelerated ash dieback plots (t-test, t = 4.8, p < 0.01) acting as a buffer, resulting in normal tree growth during drought compared to greatly reduced growth in plots with weaker dieback.These findings emphasise the complex interactions between extreme climate events and pathogen outbreaks. Better understanding of the relationships between pathogens and hydrology on tree growth is imperative and detailed long-term studies on tree growth and hydrology will facilitate and improve mitigation strategies.

Transcriptomics, proteomics, and physiological assays reveal immunosuppression in the eastern oyster Crassostrea virginica exposed to acidification stress

Ocean acidification (OA) is recognized as a major stressor for a broad range of marine organisms, particularly shell-building invertebrates. OA can cause alterations in various physiological processes such as growth and metabolism, although its effect on host-pathogen interactions remains largely unexplored. In this study, we used transcriptomics, proteomics, and physiological assays to evaluate changes in immunity of the eastern oyster Crassostrea virginica exposed to OA conditions (pH = 7.5 vs pH = 7.9) at various life stages. The susceptibility of oyster larvae to Vibrio infection increased significantly (131 % increase in mortality) under OA conditions, and was associated with significant changes in their transcriptomes. The significantly higher mortality of larvae exposed to pathogens and acidification stress could be the outcome of an increased metabolic demand to cope with acidification stress (as seen by upregulation of metabolic genes) at the cost of immune function (downregulation of immune genes). While larvae were particularly vulnerable, juveniles appeared more robust to the stressors and there were no differences in mortality after pathogen (Aliiroseovarius crassostrea and Vibrio spp.) exposure. Proteomic investigations in adult oysters revealed that acidification stress resulted in a significant downregulation of mucosal immune proteins including those involved in pathogen recognition and microbe neutralization, suggesting weakened mucosal immunity. Hemocyte function in adults was also impaired by high pCO2, with a marked reduction in phagocytosis (67 % decrease in phagocytosis) in OA conditions. Together, results suggest that OA impairs immune function in the eastern oyster making them more susceptible to pathogen-induced mortality outbreaks. Understanding the effect of multiple stressors such as OA and disease is important for accurate predictions of how oysters will respond to future climate regimes.

Seasonal changes in network connectivity and consequences for pathogen transmission in a solitary carnivore

Seasonal variation in habitat use and animal behavior can alter host contact patterns with potential consequences for pathogen transmission dynamics. The endangered Florida panther (Puma concolor coryi) has experienced significant pathogen-induced mortality and continues to be at risk of future epidemics. Prior research has found increased panther movement in Florida’s dry versus wet seasons, which may affect panther population connectivity and seasonally increase potential pathogen transmission. Our objective was to determine if Florida panthers are more spatially connected in dry seasons relative to wet seasons, and test if identified connectivity differences resulted in divergent predicted epidemic dynamics. We leveraged extensive panther telemetry data to construct seasonal panther home range overlap networks over an 11 year period. We tested for differences in network connectivity, and used observed network characteristics to simulate transmission of a broad range of pathogens through dry and wet season networks. We found that panthers were more spatially connected in dry seasons than wet seasons. Further, these differences resulted in a trend toward larger and longer pathogen outbreaks when epidemics were initiated in the dry season. Our results demonstrate that seasonal variation in behavioral patterns—even among largely solitary species—can have substantial impacts on epidemic dynamics.

Serratia marcescens induces apoptosis in Diaphorina citri gut cells via reactive oxygen species-mediated oxidative stress.

Asian citrus psyllid, Diaphorina citri, is a notorious pest in the citrus industry because it transmits Candidatus Liberibacter asiaticus, which causes an uncurable, devastating disease in citrus worldwide. Serratia marcescens is widely distributed in various environments that exhibits toxic effects to many insects. To develop strategies for enhancing the efficiency of pathogen-induced host mortality, a better understanding of the toxicity mechanism of Serratia marcescens on Diaphorina citri is critical. Serratia marcescens KH-001 successfully colonized Diaphorina citri gut by feeding artificial diets, resulting in the damage of cells including nucleus, mitochondria, vesicles, and microvilli. Oral ingestion of Serratia marcescens KH-001 strongly induced apoptosis in gut cells by enhancing levels of Cyt c, p53 and caspase-1 and decreasing levels of inhibitors of apoptosis (IAP) and Bax inhibitor-1 (BI-1). The expression of dual oxidase (Duox) and nitric oxide synthase (Nos) was up-regulated by Serratia marcescens KH-001, which increased hydrogen peroxide (H2 O2 ) levels in the gut. Injection of abdomen of Diaphorina citri with H2 O2 accelerated the death of the adults and induced apoptosis in the gut cells by activating Cyt c, p53 and caspase-1 and suppressing IAP and BI-1. Pretreatment of infected Diaphorina citri with vitamin c (Vc) increased the adult survival and diminished the apoptosis-inducing effect. The colonization of Serratia marcescens KH-001 in the guts of Diaphorina citri increased H2 O2 accumulation, leading to severe changes and apoptosis in intestinal cells, which enhanced a higher mortality level of D. citr. This study identifies the underlying virulence mechanism of Serratia marcescens KH-001 on Diaphorina citri that contributes to a widespread application in the integrated management of citrus psyllid. © 2023 Society of Chemical Industry.

Gene duplication to the Y chromosome in Trinidadian Guppies.

Differences in allele frequencies at autosomal genes between males and females in a population can result from two scenarios. First, unresolved sexual conflict over survival can produce allelic differentiation between the sexes. However, given the substantial mortality costs required to produce allelic differences between males and females at each generation, it remains unclear how many loci within the genome experience significant sexual conflict over survival. Alternatively, recent studies have shown that similarity between autosomal and Y sequences can create perceived allelic differences between the sexes. However, Y duplications are most likely in species with large nonrecombining regions, in part because they simply represent larger targets for duplications. We assessed the genomes of 120 wild-caught guppies, which experience extensive predation- and pathogen-induced mortality and have a relatively small ancestral Y chromosome. We identified seven autosomal genes that show allelic differences between male and female adults. Five of these genes show clear evidence of whole or partial gene duplication between the Y chromosome and the autosomes. The remaining two genes show evidence of partial homology to the Y. Overall, our findings suggest that the guppy genome experiences a very low level of unresolved sexual conflict over survival, and instead the Y chromosome, despite its small ancestral size and recent origin, may nonetheless accumulate genes with male-specific functions.

Pathogen-Induced Tree Mortality Modifies Key Components of the C and N Cycles with No Changes on Microbial Functional Diversity

Comunicacion oral presentada en el 1st Meeting of the Iberian Ecological Society & XIV AEET Meeting: Ecology an integrative science in the Anthropocene, celebrado del 4-7 de febrero de 2019 en la Universidad de Barcelona (UB), Barcelona, Espana

Symptom evolution following the emergence of maize streak virus.

For pathogens infecting single host species evolutionary trade-offs have previously been demonstrated between pathogen-induced mortality rates and transmission rates. It remains unclear, however, how such trade-offs impact sub-lethal pathogen-inflicted damage, and whether these trade-offs even occur in broad host-range pathogens. Here, we examine changes over the past 110 years in symptoms induced in maize by the broad host-range pathogen, maize streak virus (MSV). Specifically, we use the quantified symptom intensities of cloned MSV isolates in differentially resistant maize genotypes to phylogenetically infer ancestral symptom intensities and check for phylogenetic signal associated with these symptom intensities. We show that whereas symptoms reflecting harm to the host have remained constant or decreased, there has been an increase in how extensively MSV colonizes the cells upon which transmission vectors feed. This demonstrates an evolutionary trade-off between amounts of pathogen-inflicted harm and how effectively viruses position themselves within plants to enable onward transmission.

Handling, infectious agents and physiological condition influence survival and post-release behaviour in migratory adult coho salmon after experimental displacement.

For Pacific salmon captured and released by fisheries, post-release behaviour and survival may be influenced by their health and condition at time of capture. We sought to characterize the interactions between infectious agent burden, fish immune and stress physiology and fisheries stressors to investigate the potential for capture-mediated pathogen-induced mortality in adult coho salmon Oncorhynchus kisutch. We used radio-telemetry paired with high-throughput qPCR of non-lethal gill biopsies for infectious agents and host biomarkers from 200 tagged fish experimentally displaced and exposed to various experimental fisheries treatments (gill net entanglement, recreational angling and recreational angling with air exposure vs. non-sampled control). We characterized relationships among post-release behaviour and survival, infectious agent presence and loads, physiological parameters and transcription profiles of stress and immune genes. All infectious agents detected were endemic and in loads consistent with previous adult Pacific salmon monitoring. Individuals exposed to fisheries treatments were less likely to reach spawning habitat compared to controls, and handling duration independent of fisheries gear had a negative effect on survival. High infectious agent burden was associated with accelerated migration initiation post-release, revealing behavioural plasticity in response to deteriorating condition in this semelparous species. Prevalence and load of infectious agents increased post-migration as well as transcription signatures reflected changes in immune and stress profiles consistent with senescence. Results from this study further our understanding of factors associated with fisheries that increase risk of post-release mortality and characterize some physiological mechanisms that underpin migratory behaviour.

Shifts along the parasite-mutualist continuum are opposed by fundamental trade-offs.

Theory suggests that symbionts can readily evolve more parasitic or mutualistic strategies with respect to hosts. However, many symbionts have stable interactions with hosts that improve nutrient assimilation or confer protection from pathogens. We explored the potential for evolution of increased parasitism or decreased parasitism and mutualism in a natural gut symbiosis between larvae of Plutella xylostella and the microbe Enterobacter cloacae. We focused on interactions with the pathogen, Bacillus thuringiensis: selecting for parasitism in terms of facilitating pathogen infection, or increased mutualism in terms of host protection. Selection for parasitism led to symbionts increasing pathogen-induced mortality but reduced their competitive ability with pathogens and their in vitro growth rates. Symbionts did not evolve to confer protection from pathogens. However, several lineages evolved reduced parasitism, primarily in terms of moderating impacts on host growth, potentially because prudence pays dividends through increased host size. Overall, the evolution of increased parasitism was achievable but was opposed by trade-offs likely to reduce fitness. The evolution of protection may not have occurred because suppressing growth of B. thuringiensis in the gut might provide only weak protection or because evolution towards protective interactions was opposed by the loss of competitive fitness in symbionts.

Pathogen-induced tree mortality interacts with predicted climate change to alter soil respiration and nutrient availability in Mediterranean systems

Ecosystems worldwide must simultaneously cope with several global change drivers with potential strong effects on ecosystem functioning. These drivers might interact in unexpected ways, but our still limited understanding of these interactive effects precludes us from predicting the impact of global change on ecosystem functioning. In this study we assessed the direct effects of pathogen-induced tree mortality and predicted warming and drought on C, N and P in Mediterranean forest soils affected by the decline of their dominant tree species (i.e. Quercus suber) due to the invasive pathogen Phytophthora cinnamomi. We also explored the potential indirect effects due to species replacement after Q. suber mortality. To achieve our goal, we conducted a soil incubation experiment using soils collected under Q. suber trees with different health status (i.e. healthy, defoliated and dead trees) and from coexistent shrubs (i.e. pioneer and late successional shrubs). These soils were incubated under controlled temperatures and soil moistures, mimicking various climate change scenarios predicted for 2050 and 2100 in the Mediterranean Basin. Our results showed that P. cinnamomi-induced mortality and future warming and drought may interact to simultaneously alter biogeochemical cycles in Q. suber forest soils. Resistance of studied variables to changes in temperature and moisture tended to be lower for dead trees than for healthy and defoliated trees. Moreover, we found that soil respiration and nutrient availability might be affected indirectly by P. cinnamomi-induced mortality due to species replacement. Overall, our results support a high potential of invasive pathogen species for modifying the response of soil functioning to climatic stressors.

Mechanisms of Fish Macrophage Antimicrobial Immunity.

Overcrowding conditions and temperatures shifts regularly manifest in large-scale infections of farmed fish, resulting in economic losses for the global aquaculture industries. Increased understanding of the functional mechanisms of fish antimicrobial host defenses is an important step forward in prevention of pathogen-induced morbidity and mortality in aquaculture setting. Like other vertebrates, macrophage-lineage cells are integral to fish immune responses and for this reason, much of the recent fish immunology research has focused on fish macrophage biology. These studies have revealed notable similarities as well as striking differences in the molecular strategies by which fish and higher vertebrates control their respective macrophage polarization and functionality. In this review, we address the current understanding of the biological mechanisms of teleost macrophage functional heterogeneity and immunity, focusing on the key cytokine regulators that control fish macrophage development and their antimicrobial armamentarium.

Disturbance Alters the Relative Importance of Topographic and Biogeochemical Controls on Microbial Activity in Temperate Montane Forests

Fire and pathogen-induced tree mortality are the two dominant forms of disturbance in Western U.S. montane forests. We investigated the consequences of both disturbance types on the controls of microbial activity in soils from 56 plots across a topographic gradient one year after the 2012 High Park wildfire in Colorado. Topsoil biogeochemistry, soil CO2 efflux, potential exoenzyme activities, and microbial biomass were quantified in plots that experienced fire disturbance, beetle disturbance, or both fire and beetle disturbance, and in plots where there was no recent evidence of disturbance. Soil CO2 efflux, N-, and P-degrading exoenzyme activities in undisturbed plots were positively correlated with soil moisture, estimated from a topographic wetness index; coefficient of determinations ranged from 0.5 to 0.65. Conversely, the same estimates of microbial activities from fire-disturbed and beetle-disturbed soils showed little correspondence to topographically inferred wetness, but demonstrated mostly negative relationships with soil pH (fire only) and mostly positive relationships with DOC/TDN (dissolved organic carbon/total dissolved nitrogen) ratios for both disturbance types. The coefficient of determination for regressions of microbial activity with soil pH and DOC/TDN reached 0.8 and 0.63 in fire- and beetle-disturbed forests, respectively. Drivers of soil microbial activity change as a function of disturbance type, suggesting simple mathematical models are insufficient in capturing the impact of disturbance in forests.

Terrestrial Condition Assessment for National Forests of the USDA Forest Service in the Continental US

The terrestrial condition assessment (TCA) evaluates effects of uncharacteristic stressors and disturbance agents on land-type associations (LTAs) to identify restoration opportunities on national forest system (NFS) lands in the United States. A team of agency scientists and managers, representing a broad array of natural resource disciplines, developed a logic structure for the TCA to identify appropriate data sources to support analyses. Primary national data sources included observed insect- and pathogen-induced mortality, key critical loads for soil and the atmosphere, long term seasonal departures in temperature and precipitation, road densities, uncharacteristic wildfires, historical fire regime departure, wildfire potential, insect and pathogen risk, and vegetation departure from natural range of variability. The TCA was implemented with the ecosystem management decision support (EMDS) system, a spatial decision support system for landscape analysis and planning. EMDS uses logic models to interpret data, synthesizes information over successive layers of logic topics, and draws inferences about the ecological integrity of LTAs as an initial step to identifying high priority LTAs for landscape restoration on NFS lands. Results from the analysis showed that about 74 percent of NFS lands had moderate or better overall ecological integrity. Major impacts to ecological integrity included risk of mortality due to insects and disease, extent of current mortality, extent of areas with high and very high wildfire hazard potential, uncharacteristically severe wildfire, and elevated temperatures. In the discussion, we consider implications for agency performance reporting on restoration activities, and subsequent possible steps, including strategic and tactical planning for restoration. The objective of the paper is to describe the TCA framework with results from a national scale application on NFS lands.

Abiotic effects on the clear-winged grasshopper (Orthoptera: Acridae) and its fungal pathogen Entomophaga grylli (Entomophthorales: Entomophthoraceae) in an intermountain bunch-grass prairie

AbstractThe grasshopper, Camnula pellucida Scudder (Orthoptera: Acridae), is a severe pest of small grains and rangeland forage in North America. In a field experiment using cages containing C. pellucida in northwestern Montana, United States of America, we manipulated exposure to the fungal entomopathogen, Entomophaga grylli Fresenius (Entomophthorales: Entomophthoraceae) pathotype 1, temperature using small greenhouses, and moisture for the pathogen with water pillows. Treatment effects on fungal infection (mycosis) rates and grasshopper survivorship were assessed. Water pillows provided additional moist habitat for E. grylli without having an impact on grasshopper performance or the plant biomass and nitrogen content. Number of fungal spores, pathogen-induced mortality rates, and treatment effects on grass biomass and nitrogen content were also measured. Water pillows benefited the pathogen by increasing fungal spore levels by eightfold, which in turn shortened pathogen-exposed grasshopper survival time by half. In contrast, warming reduced fungal spore levels by 50% and subsequently reduced mortality from E. grylli by 67%. However, warmed pathogen-exposed grasshoppers did not exhibit enhanced survival, which may be due, in part, to intraspecific competition among the surviving grasshoppers.

Does Slow and Variable Recovery of Diadema antillarum on Caribbean Fore-Reefs Reflect Density-Dependent Habitat Selection?

Recovery of the Caribbean long-spined sea urchin Diadema antillarum from the pathogen-induced mass mortality event of 1983 has been slow and variable. Multiple studies indicate that post-mortality population densities are greatest in sheltered lagoon and back reef habitats, and that recovery is limited on forereefs where pre-mortality densities were also high [1-5]. We carried out detailed surveys of a recovering population of D. antillarum in Curacao to document an ongoing influence of habitat type on population density, and to explore what ecosystem characteristics might drive observed recovery patterns. We quantified D. antillarum population density, larval settlement rates, herbivorous fish biomass, algal turfs, macroalgae and predatory fish biomass in sites with and without structural complexity on reefs in sheltered lagoon and backreef locations, and on the forereef, using an orthogonal survey design. D. antillarum densities were greatest in sheltered lagoon and backreef locations, with high structural complexity. However, densities were significantly lower than those reported prior to the mass mortality event. Larval settlement rates were greater in sheltered lagoon and backreef locations but did not fully account for observed patterns in urchin density. Sheltered lagoon and backreef habitats had more turf algae and fewer herbivorous fish than forereef habitats. Predator abundance was generally low and did not differ significantly among habitat types. In light of our results, we hypothesize that patterns of D. antillarum recovery in Curacao are consistent with dynamics expected in the presence of density-dependent habitat selection. More algal resources and fewer herbivorous fish provide a mechanism for increased fitness and habitat suitability in sheltered, lagoon and backreef habitats. Forereefs, by contrast, offer reduced habitat suitability and, we hypothesize, will only be re-colonized once the carrying capacity of more favourable habitats is exceeded. We propose a number of testable predictions to explore this theory further, and advocate for including sheltered lagoon and backreef habitats in D. antillarum population surveys to monitor recovery, as well as protecting populations found in these habitats where necessary. We predict that when current populations return to pre-mortality densities, range expansion may allow for a return of D. antillarum to Caribbean forereefs.

Drosophila melanogaster does not exhibit a behavioural fever response when infected with Drosophila C virus.

Behavioural fever is a widely conserved response to infection. The host increases body temperature (Tb) by altering their preferred temperature (Tp), generating a fever and delaying or avoiding pathogen-induced mortality. This response is not ubiquitous in insects, however, although few studies have investigated this response to viral infection. Here, we examined the change in Tp of Drosophila in response to virus infection using a thermal gradient. No difference in Tp was observed. We suggest that the lack of behavioural fever could be due to the increased energy cost of maintaining a higher Tb whilst the immune response is active. To the best of our knowledge, this is the first study to assay for changes in Tp of infected Drosophila.

Pathogen evolution under host avoidance plasticity.

Host resistance consists of defences that limit pathogen burden, and can be classified as either adaptations targeting recovery from infection or those focused upon infection avoidance. Conventional theory treats avoidance as a fixed strategy which does not vary from one interaction to the next. However, there is increasing empirical evidence that many avoidance strategies are triggered by external stimuli, and thus should be treated as phenotypically plastic responses. Here, we consider the implications of avoidance plasticity for host-pathogen coevolution. We uncover a number of predictions challenging current theory. First, in the absence of pathogen trade-offs, plasticity can restrain pathogen evolution; moreover, the pathogen exploits conditions in which the host would otherwise invest less in resistance, causing resistance escalation. Second, when transmission trades off with pathogen-induced mortality, plasticity encourages avirulence, resulting in a superior fitness outcome for both host and pathogen. Third, plasticity ensures the sterilizing effect of pathogens has consequences for pathogen evolution. When pathogens castrate hosts, selection forces them to minimize mortality virulence; moreover, when transmission trades off with sterility alone, resistance plasticity is sufficient to prevent pathogens from evolving to fully castrate.

Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality

Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality

GENETIC VARIATION IN RESISTANCE AND FECUNDITY TOLERANCE IN A NATURAL HOST-PATHOGEN INTERACTION

Individuals vary in their ability to defend against pathogens. Determining how natural selection maintains this variation is often difficult, in part because there are multiple ways that organisms defend themselves against pathogens. One important distinction is between mechanisms of resistance that fight off infection, and mechanisms of tolerance that limit the impact of infection on host fitness without influencing pathogen growth. Theory predicts variation among genotypes in resistance, but not necessarily in tolerance. Here, we study variation among pea aphid (Acyrthosiphon pisum) genotypes in defense against the fungal pathogen Pandora neoaphidis. It has been well established that pea aphids can harbor symbiotic bacteria that protect them from fungal pathogens. However, it is unclear whether aphid genotypes vary in defense against Pandora in the absence of protective symbionts. We therefore measured resistance and tolerance to fungal infection in aphid lines collected without symbionts, and found variation among lines in survival and in the percent of individuals that formed a sporulating cadaver. We also found evidence of variation in tolerance to the effects of pathogen infection on host fecundity, but no variation in tolerance of pathogen-induced mortality. We discuss these findings in light of theoretical predictions about host-pathogen coevolution.

Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality

Exposure to stressors at formative stages in the development of wildlife and humans can have enduring effects on health. Understanding which, when and how stressors cause enduring health effects is crucial because these stressors might then be avoided or mitigated during formative stages to prevent lasting increases in disease susceptibility. Nevertheless, the impact of early-life exposure to stressors on the ability of hosts to resist and tolerate infections has yet to be thoroughly investigated. Here, we show that early-life, 6-day exposure to the herbicide atrazine (mean ± s.e.: 65.9±3.48 µg l(-1)) increased frog mortality 46 days after atrazine exposure (post-metamorphosis), but only when frogs were challenged with a chytrid fungus implicated in global amphibian declines. Previous atrazine exposure did not affect resistance of infection (fungal load). Rather, early-life exposure to atrazine altered growth and development, which resulted in exposure to chytrid at more susceptible developmental stages and sizes, and reduced tolerance of infection, elevating mortality risk at an equivalent fungal burden to frogs unexposed to atrazine. Moreover, there was no evidence of recovery from atrazine exposure. Hence, reducing early-life exposure of amphibians to atrazine could reduce lasting increases in the risk of mortality from a disease associated with worldwide amphibian declines. More generally, these findings highlight that a better understanding of how stressors cause enduring effects on disease susceptibility could facilitate disease prevention in wildlife and humans, an approach that is often more cost-effective and efficient than reactive medicine.