1887

Abstract

The ubiquitous unicellular eukaryote, , is known to play a role in the survival and dissemination of is the leading cause of bacterial foodborne gastroenteritis world-wide and is a major public health problem. The ability of to interact and potentially invade epithelial cells is thought to be key for disease development in humans. We examined grown under standard laboratory conditions, 11168H with that harvested from within (11168H) or (11168H), and compared their ability to invade different cell lines. harvested from within amoebae had a ~3.7-fold increase in invasiveness into T84 human epithelial cells and a striking ~11-fold increase for re-entry into cells. We also investigated the invasiveness and survivability of six diverse representative strains within spp., our results confirm that invasion and survivability is likely host-cell-dependent. Our survival assay data led us to conclude that spp. are a transient host for and that survival within amoebae pre-adapts and enhances subsequent cell invasion. This study provides new insight into interactions with amoebae and its increased invasiveness potential in mammalian hosts.

Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/R012504/1 constituent project BBS/E/F/000PR10349)
    • Principle Award Recipient: BrendanW. Wren
  • 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/micro/10.1099/mic.0.001143
2022-02-17
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/168/2/mic001143.html?itemId=/content/journal/micro/10.1099/mic.0.001143&mimeType=html&fmt=ahah

References

  1. Igwaran A, Okoh AI. Human campylobacteriosis: A public health concern of global importance. Heliyon 2019; 5:e02814 [View Article] [PubMed]
    [Google Scholar]
  2. Hilbert F, Scherwitzel M, Paulsen P, Szostak MP et al. Survival of Campylobacter jejuni under conditions of atmospheric oxygen tension with the support of Pseudomonas spp. Appl Environ Microbiol 2010; 76:5911–5917 [View Article] [PubMed]
    [Google Scholar]
  3. Olofsson J, Axelsson-Olsson D, Brudin L, Olsen B, Ellström P et al. Campylobacter jejuni actively invades the amoeba Acanthamoeba polyphaga and survives within non digestive vacuoles. PLoS One 2013; 8:e78873 [View Article] [PubMed]
    [Google Scholar]
  4. Baré J, Sabbe K, Huws S, Vercauteren D, Braeckmans K et al. Influence of temperature, oxygen and bacterial strain identity on the association of Campylobacter jejuni with Acanthamoeba castellanii. FEMS Microbiol Ecol 2010; 74:371–381 [View Article] [PubMed]
    [Google Scholar]
  5. Vieira A, Seddon AM, Karlyshev AV. Campylobacter-Acanthamoeba interactions. Microbiology (Reading) 2015; 161:933–947 [View Article] [PubMed]
    [Google Scholar]
  6. Balczun C, Scheid PL. Free-living amoebae as hosts for and vectors of intracellular microorganisms with public health significance. Viruses 2017; 9:E65 [View Article] [PubMed]
    [Google Scholar]
  7. Visvesvara GS, Moura H, Schuster FL. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol 2007; 50:1–26 [View Article] [PubMed]
    [Google Scholar]
  8. Thomas V, McDonnell G, Denyer SP, Maillard J-Y et al. Free-living amoebae and their intracellular pathogenic microorganisms: risks for water quality. FEMS Microbiol Rev 2010; 34:231–259 [View Article] [PubMed]
    [Google Scholar]
  9. Siddiqui R, Khan NA. Biology and pathogenesis of Acanthamoeba. Parasit Vectors 2012; 5:6 [View Article] [PubMed]
    [Google Scholar]
  10. Guimaraes AJ, Gomes KX, Cortines JR, Peralta JM, Peralta RHS et al. Acanthamoeba spp. as a universal host for pathogenic microorganisms: One bridge from environment to host virulence. Microbiol Res 2016; 193:30–38 [View Article] [PubMed]
    [Google Scholar]
  11. Schuppler M. How the interaction of Listeria monocytogenes and Acanthamoeba spp. affects growth and distribution of the food borne pathogen. Appl Microbiol Biotechnol 2014; 98:2907–2916 [View Article] [PubMed]
    [Google Scholar]
  12. Vieira A, Ramesh A, Seddon AM, Karlyshev AV et al. CmeABC Multidrug Efflux Pump Contributes to Antibiotic Resistance and Promotes Campylobacter jejuni Survival and Multiplication in Acanthamoeba polyphaga. Appl Environ Microbiol 2017; 83:e01600-17 [View Article] [PubMed]
    [Google Scholar]
  13. Vieira A. Acanthamoeba as a Model for the Investigation of the Molecular Mechanisms of Campylobacter jejuni Pathogenesis and Survival in the Environment Kingston University; 2017
    [Google Scholar]
  14. Jervis AJ, Butler JA, Wren BW, Linton D et al. Chromosomal integration vectors allowing flexible expression of foreign genes in Campylobacter jejuni. BMC Microbiol 2015; 15:230 [View Article] [PubMed]
    [Google Scholar]
  15. Elmi A, Watson E, Sandu P, Gundogdu O, Mills DC et al. Campylobacter jejuni outer membrane vesicles play an important role in bacterial interactions with human intestinal epithelial cells. Infect Immun 2012; 80:4089–4098 [View Article] [PubMed]
    [Google Scholar]
  16. Champion OL, Karlyshev AV, Senior NJ, Woodward M, La Ragione R et al. Insect infection model for Campylobacter jejuni reveals that O-methyl phosphoramidate has insecticidal activity. J Infect Dis 2010; 201:776–782 [View Article] [PubMed]
    [Google Scholar]
  17. Paramythiotis S, Skandamis PN. Adaptive response of bacteria: Multiple hurdles, cross tolerance and tools to illustrate underlying mechanisms. in AIP Conference Proceedings Kos, Greece: American Institute of Physics; 2015
    [Google Scholar]
  18. Murphy C, Carroll C, Jordan KN. Induction of an adaptive tolerance response in the foodborne pathogen, Campylobacter jejuni. FEMS Microbiol Lett 2003; 223:89–93 [View Article] [PubMed]
    [Google Scholar]
  19. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y et al. Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 2005; 71:20–28 [View Article] [PubMed]
    [Google Scholar]
  20. Pallen MJ, Wren BW. Bacterial pathogenomics. Nature 2007; 449:835–842 [View Article] [PubMed]
    [Google Scholar]
  21. Segal G, Shuman HA. Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect Immun 1999; 67:2117–2124 [View Article] [PubMed]
    [Google Scholar]
  22. Best A, Price C, Ozanic M, Santic M, Jones S et al. A Legionella pneumophila amylase is essential for intracellular replication in human macrophages and amoebae. Sci Rep 2018; 8:6340 [View Article] [PubMed]
    [Google Scholar]
  23. Axelsson-Olsson D, Waldenström J, Broman T, Olsen B, Holmberg M et al. Protozoan Acanthamoeba polyphaga as a potential reservoir for Campylobacter jejuni. Appl Environ Microbiol 2005; 71:987–992 [View Article] [PubMed]
    [Google Scholar]
  24. Bui XT, Winding A, Qvortrup K, Wolff A, Bang DD et al. Survival of Campylobacter jejuni in co-culture with Acanthamoeba castellanii: role of amoeba-mediated depletion of dissolved oxygen. Environ Microbiol 2012; 14:2034–2047 [View Article] [PubMed]
    [Google Scholar]
  25. Bojanić K, Acke E, Roe WD, Marshall JC, Cornelius AJ et al. Comparison of the pathogenic potential of Campylobacter jejuni, C. upsaliensis and C. helveticus and limitations of using larvae of Galleria mellonella as an infection model. Pathogens 2020; 9:713 [View Article]
    [Google Scholar]
  26. Snelling WJ, Stern NJ, Lowery CJ, Moore JE, Gibbons E et al. Colonization of broilers by Campylobacter jejuni internalized within Acanthamoeba castellanii. Arch Microbiol 2008; 189:175–179 [View Article] [PubMed]
    [Google Scholar]
  27. Konkel ME, Joens LA. Adhesion to and invasion of HEp-2 cells by Campylobacter spp. Infect Immun 1989; 57:2984–2990 [View Article] [PubMed]
    [Google Scholar]
  28. Newell DG, McBride H, Saunders F, Dehele Y, Pearson AD et al. The virulence of clinical and environmental isolates of Campylobacter jejuni. J Hyg (Lond) 1985; 94:45–54 [View Article] [PubMed]
    [Google Scholar]
  29. Everest PH, Goossens H, Butzler JP, Lloyd D, Knutton S et al. Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J Med Microbiol 1992; 37:319–325 [View Article] [PubMed]
    [Google Scholar]
  30. Kovács JK, Cox A, Schweitzer B, Maróti G, Kovács T et al. Virulence traits of inpatient Campylobacter jejuni isolates, and a transcriptomic approach to identify potential genes maintaining intracellular survival. Microorganisms 2020; 8:531 [View Article] [PubMed]
    [Google Scholar]
  31. Nale Y. Role of Acanthamoeba spp. in the environmental survival of Listeria monocytogenes University of Leicester; 2011
    [Google Scholar]
  32. Rayamajhee B, Subedi D, Peguda HK, Willcox MD, Henriquez FL et al. A systematic review of intracellular microorganisms within Acanthamoeba to understand potential impact for infection. Pathogens 2021; 10:225 [View Article] [PubMed]
    [Google Scholar]
  33. Booton GC, Visvesvara GS, Byers TJ, Kelly DJ, Fuerst PA et al. Identification and distribution of Acanthamoeba species genotypes associated with nonkeratitis infections. J Clin Microbiol 2005; 43:1689–1693 [View Article] [PubMed]
    [Google Scholar]
  34. Jercic MI, Aguayo C, Saldarriaga-Córdoba M, Muiño L, Chenet SM et al. Genotypic diversity of Acanthamoeba strains isolated from Chilean patients with Acanthamoeba keratitis. Parasit Vectors 2019; 12:58 [View Article] [PubMed]
    [Google Scholar]
  35. Burnham PM, Hendrixson DR. Campylobacter jejuni: collective components promoting a successful enteric lifestyle. Nat Rev Microbiol 2018; 16:551–565 [View Article] [PubMed]
    [Google Scholar]
  36. Bronowski C, James CE, Winstanley C. Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol Lett 2014; 356:8–19 [View Article] [PubMed]
    [Google Scholar]
  37. de Vries SP, Gupta S, Baig A, Wright E, Wedley A et al. Genome-wide fitness analyses of the foodborne pathogen Campylobacter jejuni in in vitro and in vivo models. Sci Rep 2017; 7:1251 [View Article] [PubMed]
    [Google Scholar]
  38. Karlyshev AV, Linton D, Gregson NA, Wren BW et al. A novel paralogous gene family involved in phase-variable flagella-mediated motility in Campylobacter jejuni. Microbiology (Reading) 2002; 148:473–480 [View Article] [PubMed]
    [Google Scholar]
  39. Jones MA, Marston KL, Woodall CA, Maskell DJ, Linton D et al. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect Immun 2004; 72:3769–3776 [View Article] [PubMed]
    [Google Scholar]
  40. Korlath JA, Osterholm MT, Judy LA, Forfang JC, Robinson RA et al. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 1985; 152:592–596 [View Article] [PubMed]
    [Google Scholar]
  41. Gundogdu O, da Silva DT, Mohammad B, Elmi A, Wren BW et al. The Campylobacter jejuni oxidative stress regulator RrpB is associated with a genomic hypervariable region and altered oxidative stress resistance. Front Microbiol 2016; 7:2117 [View Article] [PubMed]
    [Google Scholar]
  42. Friis C, Wassenaar TM, Javed MA, Snipen L, Lagesen K et al. Genomic characterization of Campylobacter jejuni strain M1. PLoS One 2010; 5:e12253 [View Article] [PubMed]
    [Google Scholar]
  43. Wassenaar TM, Bleumink-Pluym NM, van der Zeijst BA. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J 1991; 10:2055–2061 [View Article] [PubMed]
    [Google Scholar]
  44. Fouts DE, Mongodin EF, Mandrell RE, Miller WG, Rasko DA et al. Major structural differences and novel potential virulence mechanisms from the genomes of multiple campylobacter species. PLoS Biol 2005; 3:e15 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001143
Loading
/content/journal/micro/10.1099/mic.0.001143
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