Phylogeny, morphology, virulence, ecology, and host range of
Ordospora pajunii
(Ordosporidae), a microsporidian symbiont of
Daphnia
spp.
Authors: Dziuba Marcin K. , McIntire Kristina M. , Seto Kensuke , Davenport Elizabeth S. , Rogalski Mary A. , Gowler Camden D. , Baird Emma , Vaandrager Megan , Huerta Cristian , Jaye Riley , Corcoran Fiona E. , Withrow Alicia , Ahrendt Steven , Salamov Asaf , Nolan Matt , Tejomurthula Sravanthi , Barry Kerrie , Grigoriev Igor V. , James Timothy Y. , Duffy Meghan A. 
Published: April 2024

ABSTRACT

The 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 indicate 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
Daphnia 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.

IMPORTANCE

The 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 toward mutualism in certain ecological contexts and helps establish
O. pajunii
is a valuable model for investigating shifts along the mutualism-parasitism continuum.