A large collection of novel nematode-infecting microsporidia and their diverse interactions withC. elegansand other related nematodes
Authors: Zhang Gaotian , Sachse Martin , Prevost Marie-Christine , Luallen Robert , Troemel Emily , Félix Marie-Anne 
Published: September 2016

Microsporidia are fungi-related intracellular pathogens that may infect virtually all animals, but are poorly understood. The nematodeCaenorhabditis eleganshas recently become a model host for studying microsporidia through the identification of its natural microsporidian pathogenNematocida parisii.However, it was unclear how widespread and diverse microsporidia infections are inC. elegansor other related nematodes in the wild. Here we describe the isolation and culture of 47 nematodes with microsporidian infections.N. parisiiis found to be the most common microsporidia infectingC. elegansin the wild. In addition, we further describe and name six new species in theNematocidagenus. Our sampling and phylogenetic analysis further identify two subclades that are genetically distinct fromNematocida, and we name themEnteropsectraandPancytospora.Interestingly, unlikeNematocida,these two genera belong to the main clade of microsporidia that includes human pathogens. All of these microsporidia are horizontally transmitted and most specifically infect intestinal cells, exceptPancytospora epiphagathat replicates mostly in the epidermis of itsCaenorhabditishost. At the subcellular level in the infected host cell, spores of the novel genusEnteropsectrashow a characteristic apical distribution and exit via budding off of the plasma membrane, instead of exiting via exocytosis as spores ofNematocida.Host specificity is broad for some microsporidia, narrow for others: indeed, some microsporidia can infectOscheius tipulaebut not its sister species, and conversely. We also show thatN. ausubelifails to strongly induce inC. elegansthe transcription of genes that are induced by otherNematocidaspecies, suggesting it has evolved mechanisms to prevent induction of this host response. Altogether, these newly isolated species illustrate the diversity and ubiquity of microsporidian infections in nematodes, and provide a rich resource to investigate host-parasite coevolution in tractable nematode hosts.

Author Summary

Microsporidia are microbial parasites that live inside their host cells and can cause disease in humans and many other animals. The small nematode wormCaenorhabditis eleganshas recently become a convenient model host for studying microsporidian infections. In this work, we sampleCaenorhabditisand other small nematodes and 47 associated microsporidian strains from the wild. We characterize the parasites for their position in the evolutionary tree of microsporidia and for their lifecycle and morphology. We find several new species and genera, especially some that are distantly related to the previously knownNematocida parisiiand instead closely related to human pathogens. We find that some of these species have a narrow host range. We studied two species in detail using electron microscopy and uncover a new likely mode of exit from the host cell, by budding off the host cell plasma membrane rather than by fusion of a vesicle to the plasma membrane as inN. parisii.We also find a new species that infects the epidermis and muscles ofCaenorhabditisrather than the host intestinal cells and is closely related to human pathogens. Finally, we find that oneNematocidaspecies fails to elicit the same host response that otherNematocidaspecies do. These new microsporidia open up many windows into microsporidia biology and opportunities to investigate host-parasite coevolution in theC. eleganssystem.