1887

Abstract

Intestinal helminths and microbiota share the same anatomical niche during infection and are likely to interact either directly or indirectly. Whether intestinal helminths employ bactericidal strategies that influence their microbial environment is not completely understood.

In the present study, the hypothesis that the adult hookworm produces molecules that impair bacterial growth , is tested.

To investigate the bactericidal activity of against commensal and pathogenic bacteria.

The bactericidal effect of somatic extract and excretory-secretory products of adult on Gram-positive () and Gram-negative (, serovar Typhimurium, and ) bacteria was assessed using growth assays. Minimum inhibitory concentration and minimum bactericidal concentration assays were performed using excretory-secretory products released from the pathogen.

Broad-spectrum bactericidal activity in excretory-secretory products, but not somatic extract of adult was detected. The bactericidal activity of excretory-secretory products was concentration-dependent, maintained after heat treatment, and preserved after repeated freezing and thawing.

The results of this study demonstrate that helminths such as release molecules via their excretory-secretory pathway that have broad-spectrum bactericidal activity. The mechanisms responsible for this bactericidal activity remain to be determined and further studies aimed at isolating and identifying active bactericidal molecules are needed.

Funding
This study was supported by the:
  • Division of Research Capacity Development (Award HDID5149/KR/202)
    • Principle Award Recipient: ZilungileL. Mkhize-Kwitshana
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001762
2023-11-06
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/jmm/72/11/jmm001762.html?itemId=/content/journal/jmm/10.1099/jmm.0.001762&mimeType=html&fmt=ahah

References

  1. World Health Organisation Soil-transmitted helminth infections; 2022 https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections
  2. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet 2006; 367:1521–1532 [View Article]
    [Google Scholar]
  3. Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity. Mucosal Immunol 2018; 11:1039–1046 [View Article] [PubMed]
    [Google Scholar]
  4. Rapin A, Harris NL. Helminth-bacterial interactions: cause and consequence. Trends Immunol 2018; 39:724–733 [View Article] [PubMed]
    [Google Scholar]
  5. Walk ST, Blum AM, Ewing S-S, Weinstock JV, Young VB. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm Bowel Dis 2010; 16:1841–1849 [View Article] [PubMed]
    [Google Scholar]
  6. Rausch S, Held J, Fischer A, Heimesaat MM, Kühl AA et al. Small intestinal nematode infection of mice is associated with increased enterobacterial loads alongside the intestinal tract. PLoS One 2013; 8:e74026 [View Article] [PubMed]
    [Google Scholar]
  7. Lee SC, Tang MS, Lim YAL, Choy SH, Kurtz ZD et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl Trop Dis 2014; 8:e2880 [View Article] [PubMed]
    [Google Scholar]
  8. Reynolds LA, Smith KA, Filbey KJ, Harcus Y, Hewitson JP et al. Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes 2014; 5:522–532 [View Article] [PubMed]
    [Google Scholar]
  9. Ramanan D, Bowcutt R, Lee SC, Tang MS, Kurtz ZD et al. Helminth infection promotes colonization resistance via type 2 immunity. Science 2016; 352:608–612 [View Article] [PubMed]
    [Google Scholar]
  10. Jenkins TP, Rathnayaka Y, Perera PK, Peachey LE, Nolan MJ et al. Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition. PLoS One 2017; 12:e0184719 [View Article] [PubMed]
    [Google Scholar]
  11. Peachey LE, Castro C, Molena RA, Jenkins TP, Griffin JL et al. Dysbiosis associated with acute helminth infections in herbivorous youngstock - observations and implications. Sci Rep 2019; 9:11121 [View Article] [PubMed]
    [Google Scholar]
  12. Varyani F, Fleming JO, Maizels RM. Helminths in the gastrointestinal tract as modulators of immunity and pathology. Am J Physiol Gastrointest Liver Physiol 2017; 312:G537–G549 [View Article] [PubMed]
    [Google Scholar]
  13. Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009; 167:1–11 [View Article] [PubMed]
    [Google Scholar]
  14. Wardlaw AC, Forsyth LM, Crompton DW. Bactericidal activity in the pig roundworm Ascaris suum. J Appl Bacteriol 1994; 76:36–41 [View Article] [PubMed]
    [Google Scholar]
  15. Kato Y. Humoral defense of the nematode Ascaris suum: antibacterial, bacteriolytic and agglutinating activities in the body fluid. Zoolog Sci 1995; 12:225–230 [View Article] [PubMed]
    [Google Scholar]
  16. Abner SR, Parthasarathy G, Hill DE, Mansfield LS. Trichuris suis: detection of antibacterial activity in excretory-secretory products from adults. Exp Parasitol 2001; 99:26–36 [View Article] [PubMed]
    [Google Scholar]
  17. Midha A, Janek K, Niewienda A, Henklein P, Guenther S et al. The intestinal roundworm Ascaris suum releases antimicrobial factors which interfere with bacterial growth and biofilm formation. Front Cell Infect Microbiol 2018; 8:367 [View Article] [PubMed]
    [Google Scholar]
  18. Rausch S, Midha A, Kuhring M, Affinass N, Radonic A et al. Parasitic nematodes exert antimicrobial activity and benefit from microbiota-driven support for host immune regulation. Front Immunol 2018; 9:2282 [View Article] [PubMed]
    [Google Scholar]
  19. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth C, Roberts IS et al. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 2010; 328:1391–1394 [View Article] [PubMed]
    [Google Scholar]
  20. White RR, Artavanis-Tsakonas K. How helminths use excretory secretory fractions to modulate dendritic cells. Virulence 2012; 3:668–677 [View Article] [PubMed]
    [Google Scholar]
  21. Maizels RM. Maizels lab method: Nippostrongylus life cycle. Genome Biology 2004
    [Google Scholar]
  22. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–254 [View Article] [PubMed]
    [Google Scholar]
  23. Miles AA, Misra SS, Irwin JO. The estimation of the bactericidal power of the blood. J Hyg 1938; 38:732–749 [View Article] [PubMed]
    [Google Scholar]
  24. Kato Y, Komatsu S. ASABF, a novel cysteine-rich antibacterial peptide isolated from the nematode Ascaris suum. Purification, primary structure, and molecular cloning of cDNA. J Biol Chem 1996; 271:30493–30498 [View Article] [PubMed]
    [Google Scholar]
  25. Kato Y. Nematode antimicrobial peptides. Curr Top Pept Protein Res 2007; 8:1–10
    [Google Scholar]
  26. Minaba M, Ueno S, Pillai A, Kato Y. Evolution of ASABF (Ascaris suum antibacterial factor)-type antimicrobial peptides in nematodes: putative rearrangement of disulfide bonding patterns. Dev Comp Immunol 2009; 33:1147–1150 [View Article] [PubMed]
    [Google Scholar]
  27. Cotton S, Donnelly S, Robinson MW, Dalton JP, Thivierge K. Defense peptides secreted by helminth pathogens: antimicrobial and/or immunomodulator molecules?. Front Immunol 2012; 3:269 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001762
Loading
/content/journal/jmm/10.1099/jmm.0.001762
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error