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Abstract
Microbial pathogens often establish infection within particular niches of their host for replication. Determining how infection occurs preferentially in specific host tissues is a key aspect of understanding host-microbe interactions. Here, we describe the discovery of a natural microsporidian parasite of the nematode Caenorhabditis elegans that displays a unique tissue tropism compared to previously described parasites of this host. We characterize the life cycle of this new species, Nematocida displodere, including pathogen entry, intracellular replication, and exit. N. displodere can invade multiple host tissues, including the epidermis, muscle, neurons, and intestine of C. elegans. Despite robust invasion of the intestine very little replication occurs there, with the majority of replication occurring in the muscle and epidermis. This feature distinguishes N. displodere from two closely related microsporidian pathogens, N. parisii and N. sp. 1, which exclusively invade and replicate in the intestine. Comparison of the N. displodere genome with N. parisii and N. sp. 1 reveals that N. displodere is the earliest diverging species of the Nematocida genus. Over 10% of the proteins encoded by the N. displodere genome belong to a single species-specific family of RING-domain containing proteins of unknown function that may be mediating interactions with the host. Altogether, this system provides a powerful whole-animal model to investigate factors responsible for pathogen growth in different tissue niches.
Highlights
Pathogens infect host organisms and often establish themselves within a particular niche of the host environment in order to replicate [1,2,3]
We sampled around Paris, France, for wild nematodes infected with natural pathogens, and discovered a wild Caenorhabditis elegans that was infected
The wild-caught C. elegans we found had structures that appeared like meronts and spores in an area that is likely the epidermis (S1A Fig)
Summary
Pathogens infect host organisms and often establish themselves within a particular niche of the host environment in order to replicate [1,2,3] This niche usually resides within a particular cell type or tissue, and is commonly referred to as cellular or tissue tropism. Microsporidia represent a large phylum of obligate intracellular pathogens related to fungi, which can infect a diverse array of hosts from protists to humans [9,10,11,12]. They have features consistent with having adapted to proliferate exclusively within the host cellular environment, including greatly reduced genome sizes and the loss of true mitochondria [13]. Tropism is implied from in vitro studies based on cell types that are infected but may not reflect the true tropism within the live animal [15, 16]
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