Phylogeny, morphology, virulence, ecology, and host range ofOrdospora pajunii(Ordosporidae), a microsporidian symbiont ofDaphniaspp

Abstract

Symbiosis is increasingly recognized as a dynamic relationship, with the net outcome falling along a continuum from mutualism to parasitism. A key example of this comes from a recently discovered microsporidian symbiont ofDaphnia, the net impact of which was found to vary from negative to positive. We investigated the taxonomic position of this microsporidian and the morphology of infected hosts, as well as the virulence, ecology and host range of the symbiont; we also provide information about its culturing methods. The genetic data indicates that the microsporidian symbiont belongs toOrdospora pajunii, a newly described microsporidian parasite ofDaphnia. We show thatO. pajuniiinfection damages the gut, causing infected epithelial cells to lose microvilli and then rupture. The prevalence of this microsporidian can be high (up to 100% in the lab and 77% of adults in the field). Its overall virulence seems low in most cases, but some genotypes suffer reduced survival and reproduction. Susceptibility and virulence are strongly host-genotype dependent. We found that North AmericanO. pajuniiare able to infect multipleDaphniaspecies, including the European speciesD. longispina, as well as the genusCeriodaphnia. We propose theDaphnia-O. pajuniisymbiosis 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.

How does parasite environmental transmission stage concentration change before, during, and after disease outbreaks?

“…Daphnia spp. and C. dubia are hosts for a wide range of parasites, including bacteria, fungi, microsporidia, and viruses (Duffy et al, 2015; Dziuba et al, 2023; Ebert, 2005; Metschnikoff, 1884; Rodrigues et al, 2008). We focused on eight zooplankton species ( Daphnia ambigua , Daphnia dentifera , Daphnia dubia , Daphnia mendotae , Daphnia parvula , Daphnia pulicaria , Daphnia retrocurva , and C. dubia ) and five of their common parasites in southeastern Michigan ( M. bicuspidata , P. ramosa , S. cienkowskii , B. paedophthorum , and O. pajunii ) (Table 1).…”

“…and C. dubia (Duffy et al, 2015). O. pajunii is a microsporidium, which is an obligate intracellular parasite related to fungi; this parasite infects the gut epithelial cells of hosts (de Albuquerque et al, 2022; Dziuba et al, 2023). The route of infection for these parasites is through ingestion of spores, except for B. paedophthorum that is thought to enter the brood chamber of hosts.…”

“…For instance, we predicted that M. bicuspidata and P. ramosa spore concentrations would remain low during the summer and then increase in the fall prior to disease outbreaks (C aceres et al, 2006;Shaw et al, 2020). In contrast, we anticipated B. paedophthorum and O. pajunii spore concentrations to be highest during the warmer summer months and early fall when many hosts are infected and shedding spores at high rates (Duffy et al, 2015;Dziuba et al, 2023;Imirzian, 2016;Rogalski et al, 2021). While previous field studies have hypothesized that spore concentrations changed over time (Hall et al, 2010), none have directly investigated environmental spore dynamics.…”

“…Primers for M. bicuspidata and P. ramosa were designed using ITS and 16S sequences, respectively (Shaw, 2019), and primers for S. cienkowskii were designed using the bacterium's 16S sequence (Wale et al, 2023). We used the ITS-1 sequence for B. paedophthorum (Duffy et al, 2015) and part of the small subunit (SSU) sequence for O. pajunii (Dziuba et al, 2023) to create primers and dual-quenched probes (Appendix S1: Table S1).…”

“…In contrast with these obligate killer parasites, infection assays with zooplankton hosts and the microsporidium Ordospora pajunii and oomycete Blastulidium paedophthorum in laboratory settings suggest that infected hosts routinely shed spores into the water, generating new infections in susceptible hosts (Duffy et al, 2015;Dziuba et al, 2023). We know that all five of these common and well studied zooplankton parasites negatively affect host fitness and population dynamics (Duffy & Hall, 2008;Duffy et al, 2015;Dziuba et al, 2023;Ebert, 2000;McIntire et al, 2023). However, we do not yet know how environmental spore concentrations change over time for this ecologically important zooplankton system.…”