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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  Oscheius  sp. 3, and conversely some microsporidia found infecting  Oscheius  sp. 3 do not infect  O .  tipulae . 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.

A Large Collection of Novel Nematode-Infecting Microsporidia and Their Diverse Interactions with Caenorhabditis elegans and Other Related Nematodes