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.

Author Summary

The small roundworm Caenorhabditis elegans is an important model system for many areas of biology, but little is known about its natural ecology. We have identified an intracellular parasite from C. elegans in its natural habitat isolated near Paris and have named it Nematocida parisii, or nematode-killer from Paris. N. parisii defines a new genus and species of microsporidia. Microsporidia are ubiquitous eukaryotic pathogens that are thought to be highly reduced fungi and are emerging pathogens of humans. The microsporidian N. parisii invades and resides in C. elegans intestinal cells where it goes through a multistep life cycle and eventually escapes out of intestinal cells, leaving holes in the terminal web, an important cellular structure. We have found N. parisii and a related Nematocida species in several wild-caught roundworms, indicating that microsporidian infections may be relatively common for C. elegans in the wild. The C. elegans/N. parisii interaction provides a valuable system in which to study microsporidian infections in a whole animal, and a convenient and inexpensive system in which to screen for anti-microsporidian drugs.

Abstract

A newly identified intracellular pathogen of wild-caught Caenorhabditis elegans represents a new microsporidian species that will provide a model to study this class of pathogen in humans.