Long rDNA amplicon sequencing of insect-infecting nephridiophagids reveals their affiliation to the Chytridiomycota and a potential to switch between hosts

Jürgen F H Strassert,Vincent Hervé,Andreas Brune,Christian Wurzbacher,Renate Radek,Taraha Antany

doi:10.1038/s41598-020-79842-6

Abstract

Nephridiophagids are unicellular eukaryotes that parasitize the Malpighian tubules of numerous insects. Their life cycle comprises multinucleate vegetative plasmodia that divide into oligonucleate and uninucleate cells, and sporogonial plasmodia that form uninucleate spores. Nephridiophagids are poor in morphological characteristics, and although they have been tentatively identified as early-branching fungi based on the SSU rRNA gene sequences of three species, their exact position within the fungal tree of live remained unclear. In this study, we describe two new species of nephridiophagids (Nephridiophaga postici and Nephridiophaga javanicae) from cockroaches. Using long-read sequencing of the nearly complete rDNA operon of numerous further species obtained from cockroaches and earwigs to improve the resolution of the phylogenetic analysis, we found a robust affiliation of nephridiophagids with the Chytridiomycota—a group of zoosporic fungi that comprises parasites of diverse host taxa, such as microphytes, plants, and amphibians. The presence of the same nephridiophagid species in two only distantly related cockroaches indicates that their host specificity is not as strict as generally assumed.

Highlights

Nephridiophagids are unicellular eukaryotes that parasitize the Malpighian tubules of numerous insects
The life cycle of nephridiophagids consists of a vegetative phase with multinucleated plasmodia that multiply by division into oligonucleate and uninucleate cells, and a sporogenic phase with plasmodia that form uninucleate 5–10 μm long spores
Developmental stages occur in the lumen of the Malpighian tubules (Fig. 1a)

Summary

Introduction

Nephridiophagids are unicellular eukaryotes that parasitize the Malpighian tubules of numerous insects. Their life cycle comprises multinucleate vegetative plasmodia that divide into oligonucleate and uninucleate cells, and sporogonial plasmodia that form uninucleate spores. Using long-read sequencing of the nearly complete rDNA operon of numerous further species obtained from cockroaches and earwigs to improve the resolution of the phylogenetic analysis, we found a robust affiliation of nephridiophagids with the Chytridiomycota—a group of zoosporic fungi that comprises parasites of diverse host taxa, such as microphytes, plants, and amphibians. First discovered in honey bees (formal description of the genus Nephridiophaga)[5], they are mainly known from cockroaches and beetles[8] They infect the Malpighian tubules where especially the lumen can be densely colonised by different life cycle stages[9]. Whether the intimate association of host and parasite resulted in a cospeciation between the two partners, as it has been documented for other symbiotic relationships[19,20,21,22,23], is currently unknown and awaits investigation

Methods

Results

Conclusion