Abstract
Pathogens use a variety of secreted and surface proteins to interact with and manipulate their hosts, but a systematic approach for identifying such proteins has been lacking. To identify these ‘host-exposed’ proteins, we used spatially restricted enzymatic tagging followed by mass spectrometry analysis of Caenorhabditis elegans infected with two species of Nematocida microsporidia. We identified 82 microsporidia proteins inside of intestinal cells, including several pathogen proteins in the nucleus. These microsporidia proteins are enriched in targeting signals, are rapidly evolving and belong to large Nematocida-specific gene families. We also find that large, species-specific families are common throughout microsporidia species. Our data suggest that the use of a large number of rapidly evolving species-specific proteins represents a common strategy for microsporidia to interact with their hosts. The unbiased method described here for identifying potential pathogen effectors represents a powerful approach to study a broad range of pathogens.
Highlights
Pathogens use a variety of secreted and surface proteins to interact with and manipulate their hosts, but a systematic approach for identifying such proteins has been lacking
This study provides a foundation for further functional characterization of host-exposed microsporidian proteins, and demonstrates the utility of proximity-labelling proteomic methods to broadly identify pathogen proteins localized within host cells
To identify microsporidia proteins that come into contact with the intracellular host environment, we used the technique of spatially restricted enzymatic tagging[13]
Summary
Pathogens use a variety of secreted and surface proteins to interact with and manipulate their hosts, but a systematic approach for identifying such proteins has been lacking. A recent study chemically labelled proteins inside pathogenic bacteria and identified those that were delivered inside of host cells[12] Powerful, this approach requires that a pathogen be both culturable and genetically tractable, and it is not generally applicable to many intracellular pathogens. A number of studies have used these two targeting signals to predict the set of proteins encoded by pathogen genomes that are likely to be host-exposed[21,22] It is unclear how accurate these approaches are at identifying such proteins in microsporidia and these prediction methods do not distinguish between proteins partially or wholly outside the microsporidia cell from those directed to internal membranes or compartments[13]. Some host-exposed microsporidia proteins have been characterized[23,24,25,26,27,28,29], no comprehensive identification of such proteins has been carried that include the intracellular stage of the pathogen
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