Microsporidia Are Natural Intracellular Parasites of the Nematode Caenorhabditis elegans

Abstract

For decades the soil nematode Caenorhabditis elegans has been an important model system for biology, but little is known about its natural ecology. Recently, C. elegans has become the focus of studies of innate immunity and several pathogens have been shown to cause lethal intestinal infections in C. elegans. However none of these pathogens has been shown to invade nematode intestinal cells, and no pathogen has been isolated from wild-caught C. elegans. Here we describe an intracellular pathogen isolated from wild-caught C. elegans that we show is a new species of microsporidia. Microsporidia comprise a large class of eukaryotic intracellular parasites that are medically and agriculturally important, but poorly understood. We show that microsporidian infection of the C. elegans intestine proceeds through distinct stages and is transmitted horizontally. Disruption of a conserved cytoskeletal structure in the intestine called the terminal web correlates with the release of microsporidian spores from infected cells, and appears to be part of a novel mechanism by which intracellular pathogens exit from infected cells. Unlike in bacterial intestinal infections, the p38 MAPK and insulin/insulin-like growth factor (IGF) signaling pathways do not appear to play substantial roles in resistance to microsporidian infection in C. elegans. We found microsporidia in multiple wild-caught isolates of Caenorhabditis nematodes from diverse geographic locations. These results indicate that microsporidia are common parasites of C. elegans in the wild. In addition, the interaction between C. elegans and its natural microsporidian parasites provides a system in which to dissect intracellular intestinal infection in vivo and insight into the diversity of pathogenic mechanisms used by intracellular microbes.

Intermediate filaments in Caenorhabditis elegans

“…IFs may also provide a protective barrier against various pathogens. Thus, a discontinuous endotube with large intermittent gaps was found in worms whose intestinal cells were infected with microsporidia [Troemel et al, 2008].…”

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

“…Drechmeria coniospora, Nematocida parisii, Candida albicans) and also a nodavirus (Orsay virus) [6]. Some of the used pathogens interact with C. elegans in nature, especially the microsporidian N. parisii [7], Orsay virus [8], P. aeruginosa [9], Leucobacter sp. [10], and possibly also M. nematophilum and B. thuringiensis.…”

“…Nevertheless, a few pathogens show different infection characteristics. The microsporidian N. parisii and Orsay virus are intracellular pathogens [7,8] cuticle; the latter two via the anal region and tail, and the former mainly via the mouth, the vulva and the anus [10][11][12]. These pathogens therefore target distinct tissues to those infecting the gut.…”

The small GTPase RAB-11 directs polarized exocytosis of the intracellular pathogen N. parisii for fecal-oral transmission from C. elegans

“…C. elegans is transparent, which facilitates analysis of infection in these cells within intact animals. We recently described a natural intracellular pathogen that infects the C. elegans intestine and showed that this pathogen defines a new genus and species of microsporidia, which are obligate, fungal-related intracellular pathogens (9,10). The microsporidia phylum comprises more than 1,400 species of pathogens that can infect a wide variety of animals including humans, where they commonly infect the intestine and can cause lethal diarrhea in immunocompromised hosts (11,12).…”

“…We named the C. elegans-infecting species of microsporidia Nematocida parisii, or nematode killer from Paris, because it was isolated from wild-caught C. elegans in a compost pit near Paris and it eventually kills its host. Wild-caught Caenorhabditis nematodes infected with microsporidia have been isolated from environmental regions around the globe, indicating that microsporidia are a common cause of infection for C. elegans in the wild (9,13).…”