Population screening and transmission experiments indicate paramyxid-microsporidian co-infection in Echinogammarus marinus represents a non-hyperparasitic relationship between specific parasite strains

Yasmin Guler,Amaia Green Etxabe,Stephen Short,Alex T Ford,Peter Kille

doi:10.1038/s41598-018-22276-y

Yasmin Guler, Amaia Green Etxabe + Show 3 more

Open Access

https://doi.org/10.1038/s41598-018-22276-y

Copy DOI

Abstract

Phylogenetically distant parasites often infect the same host. Indeed, co-infections can occur at levels greater than expected by chance and are sometimes hyperparasitic. The amphipod Echinogammarus marinus presents high levels of co-infection by two intracellular and vertically transmitted parasites, a paramyxid (Paramarteilia sp. Em) and a microsporidian strain (Dictyocoela duebenum Em). This co-infection may be hyperparasitic and result from an exploitative ‘hitchhiking’ or a symbiotic relationship between the parasites. However, the best-studied amphipod species are often collected from contaminated environments and may be immune-compromised. Immune-challenged animals frequently present co-infections and contaminant-exposed amphipods present significantly higher levels of microsporidian infection. This suggests the co-infections in E. marinus may result from contaminant-associated compromised immunity. Inconsistent with hyperparasitism, we find that artificial infections transmit Paramarteilia without microsporidian. Our population surveys reveal the co-infection relationship is geographically widespread but find only chance co-infection between the Paramarteilia and another species of microsporidian, Dictyocoela berillonum. Furthermore, we identify a haplotype of the Paramarteilia that presents no co-infection, even in populations with otherwise high co-infection levels. Overall, our results do not support the compromised-immunity hypothesis but rather that the co-infection of E. marinus, although non-hyperparasitic, results from a relationship between specific Paramarteilia and Dictyocoela duebenum strains.

Highlights

Invertebrates are infected by a varied array of intracellular parasites
Consistent with the idea that both Paramarteilia and D. duebenum are predominantly vertically transmitted, no horizontal transmission was observed in animals fed infected tissue and high levels of parasite infection were found in the embryos of infected mothers
Finding comparable levels of vertical transmission in co-infected and Paramarteilia-only infected animals suggests the presence of D. duebenum does not meaningfully change the transmission efficiency of the Paramarteilia when co-infecting with D. duebenum

Summary

Introduction

Invertebrates are infected by a varied array of intracellular parasites. These include both the Paramyxida (Rhizaria, Acetosporea), an order of parasitic protists commonly referred to as paramyxeans[1,2] and Microsporidia, a diverse phylum that infect hosts from all major taxa[3]. Some microsporidians subvert the amphipod sex determination mechanism and convert males into females[4,5] This feminising capacity appears to have evolved independently in several microsporidian lineages, including strains of Nosema granulosis and Dictyocoela duebenum[4,5,6]. Given the associations between paramyxids, microsporidians and amphipod feminisation[4,8], it is possible that one of these parasites is a more efficient feminiser in any given host species or environment This scenario would allow the hitchhiker to benefit from the feminising capacity of its co-infecting parasite. Feminisation and immune suppression, or potentially some combination, rely on one or both parasites exploiting the host-manipulating capacity of its co-infecting parasite In such scenarios, co-infection would reflect a relationship that has evolved between particular parasites

Methods

Results

Conclusion