Biology subjects

Dziuba, M. K.

Publications and source records attributed to Dziuba, M. K..

5 recordsLinked to original sources

bioRxiv2024

Microsporidian coinfection reduces fitness of a fungal pathogen due to rapid host mortality

Infection outcomes can be strongly context-dependent, shifting a host-symbiont relationship along a parasitism-mutualism continuum. Numerous studies show that under stressful conditions, symbionts that are typically mutualistic can become parasitic. The reverse possibility - a parasite becoming mutualistic - has received much less study. We investigated whether the parasitic microsporidium Ordospora pajunii can become beneficial for its host Daphnia dentifera in the presence of the more virulent fungal pathogen Metschnikowia bicuspidata. We found that, even though infection with O. pajunii reduces the frequency of penetration of M. bicuspidata spores into the host body cavity, it does not improve the survival or reproduction of the host; conversely, coinfection increased the mortality of Daphnia. However, the shorter lifespan of coinfected hosts disrupted the life cycle of M. bicuspidata, greatly reducing its fitness. Thus, coinfection with both pathogens was detrimental to the host at the individual level, but might be beneficial for the host population as a result of greatly reduced production of M. bicuspidata spores. If so, this would mean that O. pajunii outbreaks should delay or prevent M. bicuspidata outbreaks. In support of this, in an analysis of dynamics of naturally occurring outbreaks in two lakes where these pathogens co-occur, we found a time lag in occurrence between O. pajunii and M. bicuspidata, with M. bicuspidata epidemics only occurring after the collapse of O. pajunii epidemics. Thus, these results suggest that the interaction between co-occurring symbionts - and the net impact of a symbiont on a host - might be qualitatively different at different scales. ImportanceUnderstanding the factors that modify infection probability and virulence is crucial for identifying the drivers of infection outbreaks and modeling disease epidemic progression, and increases our ability to control diseases and reduce the harm they cause. One factor that can strongly influence infection probability and virulence is the presence of other pathogens. However, while coexposures and coinfections are incredibly common, we still have only a limited understanding of how pathogen interactions alter infection outcomes, or whether their impacts are scale-dependent. We used a system of one host and two pathogens to show that sequential coinfection can have a tremendous impact on the host and on the infecting pathogens, and that the outcome of (co-)infection can be negative or positive depending on the focal organization level.

ecology↗

bioRxiv2023

Virulence and transmission biology of the widespread, ecologically important pathogen of zooplankton, Spirobacillus cienkowskii

Spirobacillus cienkowskii (Spirobacillus, hereafter) is a widely distributed bacterial pathogen that has significant impacts on the population dynamics of zooplankton (Daphnia spp.), particularly in months when Daphnia are asexually reproducing. Yet little is known about Spirobacillus virulence, transmission mode and dynamics. As a result, we cannot explain the dynamics of Spirobacillus epidemics in nature or use Spirobacillus as a model pathogen, despite Daphnias tractability as a model-host. Here, we work to fill these knowledge gaps experimentally. We found that Spirobacillus is among the most virulent of Daphnia pathogens, killing its host within a week and reducing host fecundity. We further found that Spirobacillus did not transmit horizontally among hosts unless the host died or was destroyed (i.e., it is an "obligate killer"). In experiments aimed at quantifying the dynamics of horizontal transmission among asexually reproducing Daphnia, we demonstrated that Spirobacillus transmits poorly in the laboratory. In mesocosms, Spirobacillus failed to generate epidemics; in experiments wherein individual Daphnia were exposed, Spirobacillus transmission success was low. In the (limited) set of conditions we considered, Spirobacillus transmission success did not change with host density or pathogen dose and declined following environmental incubation. Lastly, we conducted a field survey of Spirobacillus prevalence within egg-cases (ephippia) made by sexually reproducing Daphnia. We found Spirobacillus DNA in [~]40% of ephippia, suggesting that, in addition to transmitting horizontally among asexually reproducing Daphnia, Spirobacillus may transmit vertically from sexually reproducing Daphnia. Our work fills critical gaps in the biology of Spirobacillus and illuminates new hypotheses vis-a-vis its life-history. ImportanceSpirobacillus cienkowskii is a bacterial pathogen of zooplankton, first described in the 19th Century and recently placed in a new family of bacteria, the Silvanigrellaceae. Spirobacillus causes epidemics in lake zooplankton populations and increases the probability that zooplankton will be eaten by predators. However, little is known about how Spirobacillus transmits among hosts, its impact on host survival and reproduction (i.e., how virulent it is) in laboratory conditions and what role virulence plays in Spirobacillus life cycle. Here, we experimentally quantified Spirobacillus virulence and showed that Spirobacillus must kill its host to transmit horizontally. We also found evidence that Spirobacillus may transmit vertically via Daphnias seed-like egg cases. Our work will help scientists to (i) understand Spirobacillus epidemics, (ii) use Spirobacillus as a model pathogen for the study of host-parasite interactions and (iii) better understand the unusual group of bacteria to which Spirobacillus belongs.

microbiology↗

bioRxiv2023

Phylogeny, morphology, virulence, ecology, and host range of Ordospora pajunii (Ordosporidae),a microsporidian symbiont of Daphnia spp.

Impacts of microsporidia on host individuals are frequently subtle and can be context dependent. A key example of the latter comes from a recently discovered microsporidian symbiont of Daphnia, the net impact of which was found to shift from negative to positive based on environmental context. Given this, we hypothesized low baseline virulence of the microsporidian; here, we investigated the impact of infection on hosts in controlled conditions and the absence of other stressors. We also investigated its phylogenetic position, ecology and host range. The genetic data indicates that the symbiont is Ordospora pajunii, a newly described microsporidian parasite of Daphnia. We show that O. pajunii infection damages the gut, causing infected epithelial cells to lose microvilli and then rupture. The prevalence of this microsporidian could be high (up to 100% in the lab and 77% of adults in the field). Its overall virulence was low in most cases, but some genotypes suffered reduced survival and/or reproduction. Susceptibility and virulence were strongly host-genotype dependent. We found that North American O. pajunii were able to infect multiple Daphnia species, including the European species D. longispina, as well as Ceriodaphnia spp. Given the low, often undetectable virulence of this microsporidian, and potentially far reaching consequences of infections for the host when interacting with other pathogens or food, this Daphnia - O. pajunii symbiosis emerges as a valuable system for studying the mechanisms of context-dependent shifts between mutualism and parasitism, as well as for understanding how symbionts might alter host interactions with resources. ImportanceThe net outcome of symbiosis depends on the costs and benefits to each partner. Those can be context dependent, driving the potential for an interaction to change between parasitism and mutualism. Understanding the baseline fitness impact in an interaction can help us understand those shifts; for an organism that is generally parasitic, it should be easier for it to become a mutualist if its baseline virulence is relatively low. Recently, a microsporidian was found to become beneficial to its Daphnia hosts in certain ecological contexts, but little was known about the symbiont (including its species identity). Here, we identify it as the microsporidium Ordospora pajunii. Despite the parasitic nature of microsporidia, we found O. pajunii to be, at most, mildly virulent; this helps explain why it can shift towards mutualism in certain ecological contexts and helps establish O. pajunii is a valuable model for investigating shifts along the mutualism-parasitism continuum.

ecology↗

bioRxiv2023

Transgenerational virulence: Maternal pathogen exposure reduces offspring fitness

Pathogens can alter the phenotype not only of exposed hosts, but also of future generations. Transgenerational immune priming, where parental infection drives reduced susceptibility of offspring, has been particularly well explored, but pathogens can also alter life history traits of offspring. Here, we examined the potential for transgenerational impacts of a microsporidian pathogen, Ordospora pajunii, by experimentally measuring the impact of maternal exposure on offspring fitness in the presence and absence of parasites, and then developing mathematical models that explored the population-level impacts of these transgenerational effects. We did not find evidence of transgenerational immune priming: offspring of exposed mothers became infected at high rates, similar to offspring of unexposed mothers, and the infection burden did not differ between these two groups. We also did not find any evidence of transgenerational tolerance, where daughters of exposed mothers have higher fitness after infection. Instead, we found evidence for negative transgenerational impacts of infection: uninfected offspring of exposed mothers had substantially greater early life mortality than uninfected offspring of unexposed mothers. Offspring of exposed mothers also had reduced growth rate, fewer clutches, and fewer offspring. We propose that these observations should be considered transgenerational virulence, where a pathogen reduces the fitness of the offspring of infected hosts. Our parameterized mathematical model allowed us to explore the impacts of transgenerational virulence at the population level. If transgenerational virulence manifests as decreased reproduction or increased mortality in offspring, as we saw in the empirical portion of our study, this reduces total host density, infection prevalence, and infected host density, which could have implications for both host conservation and spillover risk. We propose that transgenerational virulence might be common and is a concept worthy of further empirical and theoretical exploration.

ecology↗

bioRxiv2022

Temperature modifies trait-mediated infection outcomes in a Daphnia-fungal parasite system

One major concern related to climate change is that elevated temperatures will drive increases in parasite outbreaks. Increasing temperature is known to alter host traits and host-parasite interactions, but we know relatively little about how these are connected mechanistically - that is, about how elevated temperatures impact the relationship between epidemiologically relevant host traits and infection outcomes. Here, we used a zooplankton-fungus (Daphnia dentifera-Metschnikowia bicuspidata) disease system to investigate whether temperature interacted with host susceptibility traits in determining infection outcomes. We did this by exposing D. dentifera to M. bicuspidata or leaving them unexposed at either control (20{degrees}C) or warming temperatures (24{degrees}C) in a fully factorial design. We found that elevated temperatures altered the physical barrier and immune responses to parasites during the initial infection process, and that infected hosts at elevated temperatures suffered a greater reduction of fecundity and lifespan. Furthermore, the relationship between a key trait - gut epithelium thickness, which is a physical barrier - and the likelihood of terminal infection reversed at warmer temperatures. Together, our results highlight the complex ways that temperatures can modulate host-parasite interactions, and the importance of considering key host susceptibility traits when predicting disease dynamics in a warmer world. This article is part of the theme issue Infectious disease and evolution in a changing world.

ecology↗