Abstract
In this article, the results of a long effort to derive valuable phylogenetic data about an extraordinary spore-like infectious particle (endocytobiont) within host amoebae (Acanthamoeba sp.) recently isolated from the contact lens and the inflamed eye of a patient with keratitis are presented. The development of these endocytobionts has already been demonstrated with electron microscopic photo sequences, leading to a relevant model of its development presented here. The molecular biological investigation following the discovery of two other Pandoravirus species within aquatic sediments in 2013 led to the taxonomic affiliation of our endocytobiont with the genus Pandoravirus. A range of endocytobionts (intracellular biofilms) have been found in recent years, among which are several viruses which obligatorily proliferate within free-living amoebae. In human medicine, foreign objects which are placed in or on humans cause problems with microorganisms in biofilms. Contact lenses are especially important, because they are known as a source of a rapid formation of biofilm. These were the first Pandoraviruses described, and because this is additionally the first documented association with humans, we have clearly demonstrated how easily such (viral) endocytobionts can be transferred to humans. This case counts as an example of parasites acting as vectors of phylogenetically different microorganisms especially when living sympatric within their biocoenosis of biofilms. As the third part of the “Pandoravirus trilogy”, it finally reveals the phylogenetic nature of these “extraordinary endocytobionts” within Acanthamoebae.
Similar content being viewed by others
References
Altschul S, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anderson G, Palermo J, Schilling J, Roth R (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301:105–107
Barker J, Lambert P, Brown M (1992) Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect Immun 61:3503–3510
Borde J, Helwig P, Hauschild O (2013) Gelenkprothesen-Infektionen. Krankenhaushygiene up2date 8:89–97
Costerton J, Cheng K, Geesy G (1978) Bacterial biofilms in nature and disease. Ann Rev Microbiol 14:435–464
De Jonckheere J (1977) Use of an axenic medium for differentiation between pathogenic an non-pathogenic Naegleria fowleri isolates. Appl Environ Microbiol 33:751–757
Fritsche T, Gautom R, Seyedirashti S, Bergeron D, Lindquist T (1993) Occurrence of bacterial endosymbionts in Acanthamoeba spp. isolated from corneal and environmental specimens and contact lenses. J Clin Microbiol 31:1122–1126
Grün A-L, Stemplewitz B, Scheid P (2014) First report of an Acanthamoeba genotype T13 isolate as etiological agent of a keratitis in humans. Parasitol Res 113(6):2395–2400. doi:10.1007/s00436-014-3918-5
Khan N (2009) Acanthamoeba, biology and pathogenesis. Caister Academic Press, Norfolk, pp 213–225
La Scola B, Audic S, Robert C, Jungjang L, De Lamballerie X, Drancourt M, Birtles R, Claverie J, Raoult D (2003) A giant virus in amoebae. Science 299:5615
Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation; speciation and morphogenesis. MIT Press, Cambridge
Mehlhorn H (2001) Encyclopedic reference of parasitology. 2. Ed. Biology, structure, function. Springer Verlag, Heidelberg, pp 362–364
Nicholas K, Nicholas H, Deerfield D (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW NEWS 4:14
Page F (1988) A new key to freshwater and soil gymnamoebae with instructions for culture. Culture collection of algae and protozoa; Freshwater Biol. Ass. Ambleside
Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertraux L, Bruley C, Garin J, Claverie J, Abergel C (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341:281–286
Scheid P (2007) Mechanism of intrusion of a microsporidian-like organism into the nucleus of host amoebae (Vannella sp.) isolated from a keratitis patient. Parasitol Res 101:1097–1102
Scheid P (2014) Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res 113(7):2407–2414. doi:10.1007/s00436-014-3932-7
Scheid P, Pressmar S, Richard G, Zöller L, Michel R (2008) An extraordinary endocytobiont in Acanthamoeba sp. isolated from a patient with keratitis. Parasitol Res 102:945–950
Scheid P, Michel R, Hauröder B (2010) Investigations of an extraordinary endocytobiont in Acanthamoeba sp.: development and replication within the host amoebae. Parasitol Res 101:1097–1102
Stothard D, Schroeder-Dietrich J, Seal D, Byers T (1999) Fluorescence oligonucleotide probes for clinical and environmental detection of Acanthamoeba and the T4 18S rRNA gene sequence type. J Clin Microbiol 37:2687–2693
Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 15:4876–4882
Wieser A, Schubert S (2011) Intra-und extrazelluläre Biofilme uropathogener E. coli. Chemother J 20:181–185
Wieser A, Guggenberger C, Pritsch M, Heesemann J (2011) A novel ex vivo set-up for dynamic long-term characterization of processes on mucosal interfaces by confocal imaging and simultaneous cytokine measurements. Cell Microbiol 13:742–751
Zaubermann N, Mutsafi Y, Halevy D, Shimoni E, Klein E, Xiao C, Sun S, Minsky A (2008) Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol 6:e114
Acknowledgments
We would like to thank R. Michel for his help and advices, M. Ferse, S. Njul and P. Hommer for their excellent assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Scheid, P., Balczun, C. & Schaub, G.A. Some secrets are revealed: parasitic keratitis amoebae as vectors of the scarcely described pandoraviruses to humans. Parasitol Res 113, 3759–3764 (2014). https://doi.org/10.1007/s00436-014-4041-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-014-4041-3