Vaandrager, M. | Search bioRxiv

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↗