Polystyrene nanoplastics differentially influence the outcome of infection by two microparasites of the host Daphnia magna

The accumulation of micro- and nanoplastic particles in freshwater bodies has given rise to much concern regarding their potential adverse effects on aquatic biota. Beyond their known effects on single species, recent experimental evidence suggests that host–parasite interactions can also be affected by environmental concentrations of micro- and nanoplastics. However, investigating the effects of contaminants in simplified infection settings (i.e. one host, one parasite) may understate their ecological relevance, considering that co-infections are common in nature. We exposed the cladoceran Daphnia magna to a fungal parasite of the haemolymph (Metschnikowia bicuspidata) and a gut microsporidium (Ordospora colligata), either in single or co-infection. In addition, Daphnia were raised individually in culture media containing 0, 5 or 50 mg l−1 of polystyrene nanoplastic beads (100 nm). Only few infections were successful at the higher nanoplastic concentration, due to increased mortality of the host. While no significant effect of the low concentration was detected on the microsporidium, the proportion of hosts infected by the fungal parasite increased dramatically, leading to more frequent co-infections under nanoplastic exposure. These results indicate that nanoplastics can affect the performance of distinct pathogens in diverging ways, with the potential to favour parasite coexistence in a common zooplanktonic host

Parasitism in a changing world: investigating the outcome of infection in freshwater zooplankton (Daphnia) under the influence of anthropogenically-derived environmental shifts

Human activity is generating environmental shifts i) at a global scale and ii) at an unprecedented pace. In addition to the release of greenhouse gases, largely responsible for the ongoing elevation of the Earth’s average surface temperature, other sources of anthropic disturbances have been associated with abrupt changes in the abiotic parameters of natural ecosystems. In particular, freshwater bodies around the globe are facing a combination of warming, eutrophication and pollution by a variety of man-made contaminants. Because the influence of the external environment can strongly dictate the outcome of host-parasite interactions, the scientific literature has expressed concern that the occurrence and severity of diseases may be favoured under the influence of such disturbances. Using a commonly occurring system of a zooplanktonic host (Daphnia sp.) and its fungal parasite (Metschnikowia bicuspidata), the present work examines four possible sources of interference between anthropogenically-derived environmental shifts and the performance of a highly virulent parasite in controlled infection assays. In Chapter 1, we examined the conjoint effects of elevated temperature and host diet quality on distinct parameters of host and parasite fitness. We showed that a 4°C elevation in water temperature could greatly affect the success of infection, though the direction of these effects varied widely across specific associations of host genotype and diet quality. When incorporated as major components of the host’s diet, cyanobacterial species generally resulted in a sharp decrease of the parasite’s reproduction. To follow up on these observations, Chapter 2 asked whether the putative antifungal effects of cyanobacteria against Metschnikowia could also apply to free-living stages of the parasite, independently of their consumption by the host. Here, prior incubation of infective stages to high concentrations of cyanobacterial extracts did not reduce the success of infection, as we suspected. However, we found similar occurrences of genotype-by-environment interactions, supporting that phytoplankton composition and host genotypic diversity are important determinants of infection success in this system. In Chapter 3, we explored a contemporary source of environmental pollution affecting freshwater bodies. We provide the first experimental evidence that polystyrene nanoplastic particles (≤ 100 nm) can modulate the outcome of infection in a zooplanktonmicroparasite system, showing that high concentrations of nanoplastics can strongly reduce the parasite’s ability to produce spores within the host. Finally, to determine how climate-associated shifts in the phenology of co-occurring parasites could influence the dynamics of infection, Chapter 4 used sequential infections between our focal parasite and a competing, less virulent microsporidium (Ordospora colligata). We found evidence for priority effects at the within-host level, suggesting that prior emergence of the microsporidium in natural populations may be detrimental to the transmission of both parasites. Overall, these results provide only few examples of enhanced parasite transmission under the influence of anthropic disturbances, rather supporting that future environmental shifts will exert strong pressure on fitness traits of both hosts and parasites in this commonly occurring freshwater assemblage.Menschliche Aktivitäten verursachen Umweltveränderungen i) auf globaler Ebene und ii) in einem noch nie dagewesenen Tempo. Neben der Freisetzung von Treibhausgasen, die weitgehend für den anhaltenden Anstieg der durchschnittlichen Oberflächentemperatur der Erde verantwortlich ist, wurden auch andere Quellen anthropogener Störungen mit abrupten Veränderungen der abiotischen Parameter natürlicher Ökosysteme in Verbindung gebracht. Vor allem Süßwasserkörper auf der ganzen Welt sind mit einer Kombination aus Erwärmung, Eutrophierung und Verschmutzung durch eine Vielzahl von anthropogenen Schadstoffen konfrontiert. Da die äußere Umgebung das Ergebnis von Wirt-Parasit-Interaktionen stark beeinflussen kann, wurde in der wissenschaftlichen Literatur die Sorge geäußert, dass das Auftreten und die Schwere von Krankheiten unter dem Einfluss solcher Störungen begünstigt werden könnten. Anhand eines häufig vorkommenden Systems aus einem zooplanktonischen Wirt (Daphnia sp.) und seinem Pilzparasiten (Metschnikowia bicuspidata) werden in der vorliegenden Arbeit vier mögliche Störquellen zwischen anthropogen bedingten Umweltveränderungen und der Leistung eines hochvirulenten Parasiten in kontrollierten Infektionstests untersucht. In Kapitel 1 untersuchten wir die gemeinsamen Auswirkungen einer erhöhten Temperatur und der Qualität der Wirtsnahrung auf verschiedene Parameter der Fitness von Wirt und Parasit. Wir konnten zeigen, dass eine Erhöhung der Wassertemperatur um 4 °C den Erfolg der Infektion stark beeinflussen kann, obwohl die Richtung dieser Auswirkungen je nach Wirtsgenotyp und Nahrungsqualität stark variiert. Wenn Cyanobakterienarten als Hauptbestandteile der Nahrung des Wirts aufgenommen wurden, führten sie im Allgemeinen zu einem starken Rückgang der Reproduktion des Parasiten. Um diese Beobachtungen weiterzuverfolgen, wurde in Kapitel 2 die Frage gestellt, ob die mutmaßliche antimykotische Wirkung von Cyanobakterien gegen Metschnikowia auch für freilebende Stadien des Parasiten gelten könnte, unabhängig von ihrem Verzehr durch den Wirt. In diesem Fall führte die vorherige Inkubation der infektiösen Stadien mit hohen Konzentrationen von Cyanobakterienextrakten nicht zu einer Verringerung des Infektionserfolgs, wie wir vermutet hatten. Wir fanden jedoch ähnliche Interaktionen zwischen Genotyp und Umgebung, was darauf hindeutet, dass die Zusammensetzung des Phytoplanktons und die Vielfalt der Wirtsgenotypen wichtige Faktoren für den Infektionserfolg in diesem System sind. In Kapitel 3 untersuchten wir eine zeitgenössische Quelle der Umweltverschmutzung, die sich auf Süßwasserkörper auswirkt. Wir erbrachten den ersten experimentellen Nachweis, dass Polystyrol-Nanoplastikpartikel (≤ 100 nm) das Ergebnis der Infektion in einem Zooplankton-Mikroparasiten-System beeinflussen können. Wir konnten zeigen, dass hohe Konzentrationen von Nanoplastik die Fähigkeit des Parasiten, Sporen im Wirt zu produzieren, stark verringern können. Um schließlich festzustellen, wie klimabedingte Verschiebungen in der Phänologie von gemeinsam auftretenden Parasiten die Infektionsdynamik beeinflussen könnten, wurden in Kapitel 4 sequenzielle Infektionen zwischen unserem Hauptparasiten und einem konkurrierenden, weniger virulenten Mikrosporidium (Ordospora colligata) durchgeführt. Wir fanden Belege für Prioritätseffekte innerhalb des Wirts, was darauf hindeutet, dass ein früheres Auftreten des Mikrosporidiums in natürlichen Populationen für die Übertragung beider Parasiten nachteilig sein könnte. Insgesamt liefern diese Ergebnisse nur wenige Beispiele für eine verstärkte Parasitenübertragung unter dem Einfluss anthropogener Störungen, was eher dafür spricht, dass künftige Umweltveränderungen einen starken Druck auf die Fitnessmerkmale sowohl der Wirte als auch der Parasiten in dieser häufig vorkommenden Süßwassergemeinschaft ausüben werden

Prior exposure of a fungal parasite to cyanobacterial extracts does not impair infection of its Daphnia host

Cyanobacteria periodically dominate phytoplankton composition in lakes, and produce a wide array of toxic secondary metabolites. Blooms of cyanobacteria often coincide with infections of zooplankton by microparasites (such as Metschnikowia bicuspidata, a parasitic yeast of Daphnia), and prior research has shown that cyanobacteria-based diets could mitigate fungal infections of the host. Here, we tested whether cyanotoxins could exert detrimental effects against free-living parasite stages: we inoculated two genotypes of the host Daphnia galeata × longispina with fungal spores, which were previously exposed to cyanobacterial extracts or to a placebo solution. Additionally, to test for interactive effects of cyanotoxins through environmental exposure and host consumption, Daphnia from each treatment were fed using either green algae or the same cyanobacterium. Exposing spores to cyanobacterial extracts did not reduce their infectivity; instead, parasite infectivity was increased, but only on one host genotype. The effect of host diet on parasite growth was also host-genotype dependent, with only one Daphnia genotype showing impaired spore production under a toxic diet. Our results suggest that dissolved cyanobacterial compounds released during blooms may not exert any detrimental effect on fungal spore banks, but likely influence transmission of the parasite when incorporated as part of the host’s diet

Can climate warming save Daphnia from parasites? Reduced parasite prevalence in Daphnia populations from artificially heated lakes

Climate warming might modify infection outcomes and it has been proposed that temperature increase will result in a “sicker world.” We tested this hypothesis by comparing the prevalence of infection in a common freshwater host–parasite system (crustacean Daphnia infected with the ichthyosporean pathogen Caullerya mesnili) between five artificially heated lakes and four nearby non‐heated control lakes. The heated lakes, which receive warm water from two power plants, have experienced an elevation in water temperature of ca. 3–4°C for the last 60 yr. Analyses of 5 yr of field data revealed that Daphnia communities from heated lakes had lower parasite prevalence than communities from control sites. To disentangle a possible direct detrimental effect of elevated temperature on the parasite from differences in baseline levels of host resistance, we compared infection susceptibility between Daphnia clones isolated from heated and control lakes, under laboratory conditions at two different temperatures. Daphnia from heated lakes were less susceptible to infection than clones from control lakes, while experimental temperature did not affect infection outcome. The data did not confirm the “warmer hence sicker world” scenario. Instead, it seems that indirect effects of temperature elevation (via shifts in lake hydrology) may restrict its spread into heated lakes. Then, local adaptation to the host from control lakes further inhibits re‐establishment of the parasite from control to heated lakes. Our results underline the context‐dependency of the impact of temperature increase on host–parasite interactions.Deutsche Forschungsgemeinschaft http://dx.doi.org/10.13039/501100001659Deutscher Akademischer Austauschdienst http://dx.doi.org/10.13039/501100001655Fundacja Uniwersytetu im. Adama Mickiewicza http://dx.doi.org/10.13039/100016906Ministerstwo Nauki i Szkolnictwa Wyższego http://dx.doi.org/10.13039/501100004569Narodowe Centrum Nauki http://dx.doi.org/10.13039/50110000428

Prior exposure of a fungal parasite to cyanobacterial extracts does not impair infection of its Daphnia host

Manzi F, Agha R, Mühlenhaupt M, Wolinska J. Prior exposure of a fungal parasite to cyanobacterial extracts does not impair infection of its Daphnia host. Hydrobiologia. 2022.**Abstract** Cyanobacteria periodically dominate phytoplankton composition in lakes, and produce a wide array of toxic secondary metabolites. Blooms of cyanobacteria often coincide with infections of zooplankton by microparasites (such asMetschnikowia bicuspidata, a parasitic yeast ofDaphnia), and prior research has shown that cyanobacteria-based diets could mitigate fungal infections of the host. Here, we tested whether cyanotoxins could exert detrimental effects against free-living parasite stages: we inoculated two genotypes of the hostDaphnia galeata × longispinawith fungal spores, which were previously exposed to cyanobacterial extracts or to a placebo solution. Additionally, to test for interactive effects of cyanotoxins through environmental exposure and host consumption,Daphniafrom each treatment were fed using either green algae or the same cyanobacterium. Exposing spores to cyanobacterial extracts did not reduce their infectivity; instead, parasite infectivity was increased, but only on one host genotype. The effect of host diet on parasite growth was also host-genotype dependent, with only oneDaphniagenotype showing impaired spore production under a toxic diet. Our results suggest that dissolved cyanobacterial compounds released during blooms may not exert any detrimental effect on fungal spore banks, but likely influence transmission of the parasite when incorporated as part of the host’s diet

Can climate warming save Daphnia from parasites? Reduced parasite prevalence in Daphnia populations from artificially heated lakes

Climate warming might modify infection outcomes and it has been proposed that temperature increase will result in a “sicker world.” We tested this hypothesis by comparing the prevalence of infection in a common freshwater host–parasite system (crustacean Daphnia infected with the ichthyosporean pathogen Caullerya mesnili) between five artificially heated lakes and four nearby non-heated control lakes. The heated lakes, which receive warm water from two power plants, have experienced an elevation in water temperature of ca. 3–4°C for the last 60 yr. Analyses of 5 yr of field data revealed that Daphnia communities from heated lakes had lower parasite prevalence than communities from control sites. To disentangle a possible direct detrimental effect of elevated temperature on the parasite from differences in baseline levels of host resistance, we compared infection susceptibility between Daphnia clones isolated from heated and control lakes, under laboratory conditions at two different temperatures. Daphnia from heated lakes were less susceptible to infection than clones from control lakes, while experimental temperature did not affect infection outcome. The data did not confirm the “warmer hence sicker world” scenario. Instead, it seems that indirect effects of temperature elevation (via shifts in lake hydrology) may restrict its spread into heated lakes. Then, local adaptation to the host from control lakes further inhibits re-establishment of the parasite from control to heated lakes. Our results underline the context-dependency of the impact of temperature increase on host–parasite interactions.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/175762/1/lno12257_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/175762/2/lno12257.pd

Sequential infection of Daphnia magna by a gut microsporidium followed by a haemolymph yeast decreases transmission of both parasites

Over the course of seasonal epidemics, populations of susceptible hosts may encounter a wide variety of parasites. Parasite phenology affects the order in which these species encounter their hosts, leading to sequential infections, with potentially strong effects on within-host growth and host population dynamics. Here, the cladoceran Daphnia magna was exposed sequentially to a haemolymph-infecting yeast (Metschnikowia bicuspidata) and a gut microsporidium (Ordospora colligata), with experimental treatments reflecting two possible scenarios of parasite succession. The effects of single and co-exposure were compared on parasite infectivity, spore production and the overall virulence experienced by the host. We show that neither parasite benefited from coinfection; instead, when hosts encountered Ordospora, followed by Metschnikowia, higher levels of host mortality contributed to an overall decrease in the transmission of both parasites. These results showcase an example of sequential infections generating unilateral priority effects, in which antagonistic interactions between parasites can alleviate the intensity of infection and coincide with maladaptive levels of damage inflicted on the host

Temperature and host diet jointly influence the outcome of infection in a Daphnia‐fungal parasite system

1. Climate change has the potential to shape the future of infectious diseases, both directly and indirectly. In aquatic systems, for example, elevated temperatures can modulate the infectivity of waterborne parasites and affect the immune response of zooplanktonic hosts. Moreover, lake warming causes shifts in the communities of primary producers towards cyanobacterial dominance, thus lowering the quality of zooplankton diet. This may further affect host fitness, resulting in suboptimal resources available for parasite growth. 2. Previous experimental studies have demonstrated the respective effects of temperature and host diet on infection outcomes, using the zooplankter Daphnia and its microparasites as model systems. Although cyanobacteria blooms and heat waves are concurrent events in nature, few attempts have been made to combine both stressors in experimental settings. 3. Here, we raised the zooplankter Daphnia (two genotypes) under a full factorial design with varying levels of temperature (the standard 19°C and elevated 23°C), food quality (Scenedesmus obliquus as high‐quality green algae, Microcystis aeruginosa and Planktothrix agardhii as low‐quality cyanobacteria) and exposed them to the parasitic yeast Metschnikowia bicuspidata. We recorded life history parameters of the host as well as parasite traits related to transmission. 4. The combination of low‐quality cyanobacterial diets and elevated temperature resulted in additive detrimental effects on host fecundity. Low‐quality diets reduced parasite output, while temperature effects were context dependent. Overall, we argue that the combined effects of elevated water temperature and poor‐quality diets may decrease epidemics of a common fungal parasite under a climate change scenario