A large collection of novel nematode-infecting microsporidia and their diverse interactions withC. elegansand other related nematodes

Abstract

Microsporidia are fungi-related intracellular pathogens that may infect virtually all animals, but are poorly understood. The nematode Caenorhabditis elegans has recently become a model host for studying microsporidia through the identification of its natural microsporidian pathogen Nematocida parisii. However, it was unclear how widespread and diverse microsporidia infections are in C. elegans or other related nematodes in the wild. Here we describe the isolation and culture of 47 nematodes with microsporidian infections. N. parisii is found to be the most common microsporidia infecting C. elegans in the wild. In addition, we further describe and name six new species in the Nematocida genus. Our sampling and phylogenetic analysis further identify two subclades that are genetically distinct from Nematocida, and we name them Enteropsectra and Pancytospora. Interestingly, unlike Nematocida, 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, except Pancytospora epiphaga that replicates mostly in the epidermis of its Caenorhabditis host. At the subcellular level in the infected host cell, spores of the novel genus Enteropsectra show a characteristic apical distribution and exit via budding off of the plasma membrane, instead of exiting via exocytosis as spores of Nematocida. Host specificity is broad for some microsporidia, narrow for others: indeed, some microsporidia can infect Oscheius tipulae but not its sister species, and conversely. We also show that N. ausubeli fails to strongly induce in C. elegans the transcription of genes that are induced by other Nematocida species, 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 worm Caenorhabditis elegans has recently become a convenient model host for studying microsporidian infections. In this work, we sample Caenorhabditis and 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 known Nematocida parisii and 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 in N. parisii. We also find a new spec...

A Model for Evolutionary Ecology of Disease: The Case for Caenorhabditis Nematodes and Their Natural Parasites

“…Additional sampling has isolated multiple strains of N. parisii, as well as new microsporidian species that infect C. elegans and its relatives. They vary in their host range (Zhang et al, 2016), virulence (Balla et al, 2016), and tissue tropism (Luallen et al, 2016). Nematocida displodere primarily replicates in the muscle and epidermis, producing large numbers of spores that are trapped within the host body.…”

“…Species within the genus differ in fundamental ways such as mating system (Kiontke and Fitch, 2005;Kiontke et al, 2011), genome size (Fierst et al, 2015), genetic variation (Thomas and Wilson, 1991;Graustein et al, 2002;Jovelin et al, 2003), life span (McCulloch and Gems, 2003), ecology (Kiontke and Sudhaus, 2006), and body size (Woodruff et al, 2017). These different taxa nonetheless share many of the same types of parasites (Felix et al, 2011;Zhang et al, 2016). We can thus ask about the impact of genotypic and phenotypic variation in hosts on disease spread, e.g., does parasite epidemiology differ between selfing species (C. elegans, briggsae, tropicalis) and obligately outcrossing species (e.g., C. remanei, brenneri, japonica, drosophilae)?…”

“…Sympatry of host species suggests a community ecology approach (F elix and Duveau, 2012): Does increasing diversity of host species in a community limit disease spread? Generalist parasites seem to be shared between sympatric taxa, notably C. elegans and C. briggsae (F elix and Duveau, 2012;Zhang et al, 2016). This observation raises the question: Do hosts differ in their suitability as hosts of generalist parasites (as in Zhang et al, 2016)?…”

“…Generalist parasites seem to be shared between sympatric taxa, notably C. elegans and C. briggsae (F elix and Duveau, 2012;Zhang et al, 2016). This observation raises the question: Do hosts differ in their suitability as hosts of generalist parasites (as in Zhang et al, 2016)? Again, experimental tools can pull apart confounding variables in field data and differentiate cause from effect.…”