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

Journal Article · 11 June 2024 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.00582-24 · OSTI ID:2340228

Dziuba, Marcin K.  ^[1]; McIntire, Kristina M. ^[1]; Seto, Kensuke ^[2]; Davenport, Elizabeth S. ^[1]; Rogalski, Mary A. ^[3]; Gowler, Camden D. ^[1]; Baird, Emma ^[1]; Vaandrager, Megan ^[1]; Huerta, Cristian ^[1]; Jaye, Riley ^[1]; Corcoran, Fiona E. ^[1]; Withrow, Alicia ^[4]; Ahrendt, Steven ^[5]; Salamov, Asaf ^[5]; Nolan, Matt ^[5]; Tejomurthula, Sravanthi ^[5]; Barry, Kerrie ^[5]; Grigoriev, Igor V. ^[6]; James, Timothy Y.  ^[1]; Duffy, Meghan A. ^[1] ; Pujol, ed., Nathalie; Sinkins, ed., Steven P.

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1. Department of Ecology &, Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
2. Faculty of Environment and Information Sciences, Yokohama National University, Yokohama, Kanagawa, Japan
3. Department of Ecology &, Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA, Biology Department, Bowdoin College, Brunswick, Maine, USA
4. Center for Advanced Microscopy, Michigan State University, East Lansing, Michigan, USA
5. United States Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
6. United States Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA, Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California, USA

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.

• Sponsoring Organization: USDOE
• Grant/Contract Number: AC02-05CH11231
• OSTI ID: 2340228
• Alternate ID(s): OSTI ID: 2405928
• Journal Information: mBio (Online), Journal Name: mBio (Online) Journal Issue: 6 Vol. 15; ISSN 2150-7511
• Publisher: American Society for MicrobiologyCopyright Statement
• Country of Publication: United States
• Language: English