Excretory-secretory products from the brown stomach worm, Teladorsagia circumcincta, exert antimicrobial activity in in vitro growth assays

Authors Organisations
  • James Rooney(Author)
    University of Cambridge
  • Tim Williams(Author)
    University of Cambridge
  • Holly Marie Northcote(Author)
  • Fiona Frankl(Author)
    University of Cambridge
  • Daniel Price(Author)
    Moredun Research Institute
  • Alasdair Nisbet(Author)
    Moredun Research Institute
  • Russ Morphew(Author)
  • Cinzia Cantacessi(Author)
    University of Cambridge
Type Article
Original languageEnglish
Article number354
Number of pages15
JournalParasites & Vectors
Volume15
Issue number1
Early online date02 Oct 2022
DOI
Publication statusPublished - 01 Dec 2022
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Abstract

Background
Over the past decade, evidence has emerged of the ability of gastrointestinal (GI) helminth parasites to alter the composition of the host gut microbiome; however, the mechanism(s) underpinning such interactions remain unclear. In the current study, we (i) undertake proteomic analyses of the excretory-secretory products (ESPs), including secreted extracellular vesicles (EVs), of the ‘brown stomach worm’ Teladorsagia circumcincta, one of the major agents causing parasite gastroenteritis in temperate areas worldwide; (ii) conduct bioinformatic analyses to identify and characterise antimicrobial peptides (AMPs) with putative antimicrobial activity; and (iii) assess the bactericidal and/or bacteriostatic properties of T. circumcincta EVs, and whole and EV-depleted ESPs, using bacterial growth inhibition assays.

Methods
Size-exclusion chromatography was applied to the isolation of EVs from whole T. circumcincta ESPs, followed by EV characterisation via nanoparticle tracking analysis and transmission electron microscopy. Proteomic analysis of EVs and EV-depleted ESPs was conducted using liquid chromatography-tandem mass spectrometry, and prediction of putative AMPs was performed using available online tools. The antimicrobial activities of T. circumcincta EVs and of whole and EV-depleted ESPs against Escherichia coli were evaluated using bacterial growth inhibition assays.

Results
Several molecules with putative antimicrobial activity were identified in both EVs and EV-depleted ESPs from adult T. circumcincta. Whilst exposure of E. coli to whole ESPs resulted in a significant reduction of colony-forming units over 3 h, bacterial growth was not reduced following exposure to worm EVs or EV-depleted ESPs.

Conclusions
Our data points towards a bactericidal and/or bacteriostatic function of T. circumcincta ESPs, likely mediated by molecules with antimicrobial activity.

Keywords

  • Research, Teladorsagia circumcincta, Gastrointestinal helminth, Ruminant, Microbiome, Extracellular vesicle, Antimicrobial peptide, Excretory-secretory products

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