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Background  The primary cause of parasitic gastroenteritis in small ruminants in temperate regions is the brown stomach worm,  Teladorsagia circumcincta . Host immunity to this parasite is slow to develop, consistent with the ability of  T. circumcincta  to suppress the host immune response. Previous studies have shown that infective fourth-stage  T. circumcincta  larvae produce excretory–secretory products that are able to modulate the host immune response. The objective of this study was to identify immune modulatory excretory–secretory proteins from populations of fourth-stage  T. circumcincta  larvae present in two different host-niches: those associated with the gastric glands (mucosal-dwelling larvae) and those either loosely associated with the mucosa or free-living in the lumen (lumen-dwelling larvae).    Results  In this study excretory–secretory proteins from mucosal-dwelling and lumen-dwelling  T. circumcincta  fourth stage larvae were analysed using comparative 2-dimensional gel electrophoresis. A total of 17 proteins were identified as differentially expressed, with 14 proteins unique to, or enriched in, the excretory–secretory proteins of mucosal-dwelling larvae. One of the identified proteins, unique to mucosal-dwelling larvae, was a putative peroxiredoxin ( T. circumcincta  peroxiredoxin 1, Tci-Prx1). Peroxiredoxin orthologs from the trematode parasites  Schistosoma mansoni  and  Fasciola hepatica  have previously been shown to alternatively activate macrophages and play a key role in promoting parasite induced Th2 type immunity. Here we demonstrate that  Tci-Prx1  is expressed in all infective  T. circumcincta  life-stages and, when produced as a recombinant protein, has peroxidase activity, whereby hydrogen peroxide (H 2 O 2 ) is reduced and detoxified. Furthermore, we use an  in vitro  macrophage stimulation assay to demonstrate that, unlike peroxiredoxins from trematode parasites  Schistosoma mansoni  and  Fasciola hepatica , Tci-Prx1 is unable to alternatively activate murine macrophage cells.    Conclusions  In this study, we identified differences in the excretory–secretory proteome of mucosal-dwelling and lumen-dwelling infective fourth-stage  T. circumcincta  larvae, and demonstrated the utility of this comparative proteomic approach to identify excretory–secretory proteins of potential importance for parasite survival and/or host immune modulation.    Electronic supplementary material  The online version of this article (10.1186/s13071-019-3593-6) contains supplementary material, which is available to authorized users.

Characterisation of a niche-specific excretory–secretory peroxiredoxin from the parasitic nematode Teladorsagia circumcincta