Skip to main content

Advertisement

Log in

Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms

  • Review
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In addition to their role as parasites, free-living amoebae (FLA) can act as hosts of and vehicles for phylogentically diverse microorganisms while some of them replicate intracellularly. These microorganisms are adapted to the intracellular conditions in the amoeba, find suitable conditions and protection from negative environmental influences and take advantage of the dispersal in the environment by their amoebic host. It is expedient to call these organisms “endocytobionts”, at least during the initial steps of any studies. By doing so, it is not necessary to go into potential characteristics of these relationships such as parasitism, phoresy, zoochory, or mutualism at an early stage of study. Among those organisms resisting the lysis within their amoebic host, there are obligate and facultative pathogenic microorganisms affecting the health of humans or animals. FLA-endocytobiont relationships are not only important for the tenacity of the involved microorganisms. Especially if FLA are present in biofilms and there are close ties with many other microorganisms, the odds are for some of these microorganisms to develop human pathogenic properties. Here, the amoebic passage seems to be a prerequisite for the development of virulence factors and it may have an impact on evolutionary processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abd H (2006) Interaction between waterborne pathogenic bacteria and Acanthamoeba castellanii. Dissertation; Medical university Stockholm; Karolinska Institute

  • Adeleke A, Fields B, Benson R, Daneshvar M, Pruckler J, Ratcliff R, Harrison T, Weyant R, Birtles R, Raoult D, Halablab M (2001) Legionella drozanskii sp. nov., Legionella rowbothamii sp. nov. and Legionella fallonii sp. nov.: three unusual new Legionella species. Int J Syst Evol Microbiol 51:1151–1160

    Article  CAS  PubMed  Google Scholar 

  • Akya A, Pointon A, Thomas C (2009) Mechanism involved in phagocytosis and killing of Listeria monocytogenes by Acanthamoeba polyphaga. Parasitol Res 105:1375–1383

    Article  PubMed  Google Scholar 

  • Alsam S, Khan N (2009) Methicillin resistant Staphylococcus aureus interactions with Acanthamoeba; abstract booklet Free Living Amoebae (FLAM) meeting, Teneriffa

  • Amann R, Springer N, Schönhuber W, Ludwig W, Schmid E, Müller K-D, Michel R (1997) Obligate intracellular bacterial parasites of Acanthamoebae related to Chlamydia spp. Appl Environ Microbiol 63:115–121

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arslan D, Legendre M, Seltzer V, Abergel C, Claverie J (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci U S A 108:17486–17491

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Barker J, Humphrey T, Brown M (1999) Survival of Escherichia coli O157 in a soil protozoan: implications for disease. FEMS Microbiol Lett 173:291–295

    Article  CAS  PubMed  Google Scholar 

  • Borde J, Helwig P, Hauschild O (2013) Gelenkprothesen-Infektionen. Krankenhaushygiene up2date 8:89–97

    Article  Google Scholar 

  • Boulanger C, Edelstein P (1995) Precision and accuracy of recovery of Legionella pneumophila from seeded tap water by filtration and centrifugation. Appl Environ Microbiol 61:1805–1809

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boyer L, Yutin N, Pagnier I, Barassi L, Fournous G, Espinosa L, Robert C, Azza S, Sun S, Rossmann M, Suzan-Monti M, La Scola B, Koonin E, Raoult D (2009) Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci U S A 106:21848–21853

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cirillo J, Falkow S, Tompkins L, Bermudez L (1997) Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 65:3759–3767

    CAS  PubMed Central  PubMed  Google Scholar 

  • Collingro A, Poppert S, Heinz E, Schmitz-Esser S, Essig A, Schweikert M, Wagner M, Horn M (2005) Recovery of an environmental Chlamydia strain from activated sludge by cocultivation with Acanthamoeba sp. Microbiology 151:301–309

    Article  CAS  PubMed  Google Scholar 

  • Colson P, Pagnier I, Yoosuf N, Fournous G, La Scola B, Raoult D (2013) “Marseilleviridae”, a new family of giant viruses infecting amoebae. Arch Virol 158:915–920

    Article  CAS  PubMed  Google Scholar 

  • Corsaro D, Müller K-D, Michel R (2013) Molecular characterization and ultrastructure of a new amoeba endoparasite belonging to the Stenotrophomonas maltophilia complex. Exp Parasitol 133:383–390

    Article  CAS  PubMed  Google Scholar 

  • Dey R, Hoffmann P, Glomski J (2012) Germination and amplification of anthrax spores by soil-dwelling amoebas. Appl Environ Microbiol 78:8075–8081

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Drancourt M, Akedambi T, Raoult D (2007) Interactions between Mycobacterium xenopi, amoeba and human cells. J Hosp Infect 65:138–142

    Article  CAS  PubMed  Google Scholar 

  • Drozanski W (1956) Fatal bacterial infection in soil amoebae. Acta Microbiol Pol 5:315–317

    CAS  PubMed  Google Scholar 

  • Drozanski W (1991) Sarcobium lyticum gen. nov., sp. nov., an obligate intracellular bacterial parasite of small free-living amoebae. Int J Syst Bacteriol 41:82–87

    Article  Google Scholar 

  • English J, Parry J, Pickup R (2002) The potential for interactions between protozoa and coliform bacteria in biofilms. Conference booklet BSSP conference; London

  • Essig A, Heinemann M, Simnacher U, Marre R (1997) Infection of Acanthamoeba castellanii by Chlamydia pneumoniae. Appl Environ Microbiol 63:1396–1399

    CAS  PubMed Central  PubMed  Google Scholar 

  • Everett K, Bush R, Anderssen A (1999) Embedded description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five species, and standards for the identification of organisms. Int J Syst Bacteriol 49:415–440

    Article  CAS  PubMed  Google Scholar 

  • Flemming H (1994) Biofilme, Biofouling und mikrobielle Materialschädigung. Stuttgarter Siedlungswasserwirtschaftliche Berichte 129; Oldenburg Verlag; München

  • Fritsche T, Sobek D, Gautom R (1998) Enhancement of in vitro cytopathogenicity by Acanthamoeba spp. following acquisition of bacterial endosymbionts. FEMS Microbiol Lett 166:231–236

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Couso H, Paniagua-Crespo E, Ares-Mazas E (2007) Acanthamoeba as temporal vehicle of Cryptosporidium. Parasitol Res 100:1151–1154

    Article  CAS  PubMed  Google Scholar 

  • Greub G, Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17:413–433

    Article  PubMed Central  PubMed  Google Scholar 

  • Gustafsson K (1989) Growth and survival of four strains of Francisella tularensis in a rich medium preconditioned with Acanthamoeba palestinensis. Can J Microbiol 35:1100–1104

    Article  CAS  PubMed  Google Scholar 

  • Hägele S, Köhler R, Merkert H, Schleicher M, Hacker J, Steinert M (2000) Dictyostelium dicoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2:165–171

    Article  PubMed  Google Scholar 

  • Heinz E, Kolarov J, Kästner C, Toenshoff E, Wagner M, Horn M (2007) An Acanthamoeba sp. containing two phylogenetically different bacterial endosymbionts. Environ Microbiol 9:1604–1609

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Henning K, Zöller L, Hauröder B, Hotzel H, Michel R (2007) Hartmannella vermiformis (Hartmannellidae) harboured a hidden Chlamydia-like endosymbiont. Endocytobio Cell Res 18:1–10

    Google Scholar 

  • Hoffmann R, Michel R (2001) Distribution of free-living amoebae (FLA) during preparation and supply of drinking water. Int J Hyg Environ Health 203:215–219

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann R, Michel R, Müller K-D, Schmid E (1998) Archaea-like endocytobiotic organisms isolated from Acanthamoeba sp. (Gr II). Endo Cell Res 12:185–188

    Google Scholar 

  • Hookey J, Saunders N, Fry N, Birtles R, Harrison T (1996) Phylogeny of Legionellaceae based on small-subunit ribosomal DNA sequences and proposal of Legionella lytica comb. nov. for Legionella-like amoebal pathogens. Int J Syst Bacteriol 46:526–531

    Article  CAS  Google Scholar 

  • Horn M, Fritsche T, Gautom R, Schleifer K, Wagner M (1999) Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ Microbiol 1:357–367

    Article  CAS  PubMed  Google Scholar 

  • Horn M, Wagner M, Müller K-D, Schmid E, Fritsche T, Schleifer K-H, Michel R (2000) Neochlamydia hartmannellae gen. nov., sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. Microbiology 146:1231–1239

    CAS  PubMed  Google Scholar 

  • Horn M, Harzenetter M, Linner T, Schmid E, Müller K-D, Michel R, Wagner M (2001) Members of the Cytophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of Candidatus Amoebophilus asiaticus. Environ Microbiol 3:440–449

    Article  CAS  PubMed  Google Scholar 

  • Horn M, Fritsche T, Linner T, Gautom R, Harznetter M, Wagner M (2002) Obligate bacterial endosymbionts of Acantamoeba spp. related to the beta-Proteobacteria: proposal of candidatus Procabacter acanthamoebae gen. nov., sp. nov. Int J Syst Evol Microbiol 52:599–605

    PubMed  Google Scholar 

  • Jadin J, Francois J, Bisoux M, Languillon J, Moris R (1968) Dévelopment intranucléaire de Mycobacterium leprae dans les cellules histiocytaires chez l’animal. Bull Acad Nat Med 152:7–8

    Google Scholar 

  • Kahane S, Dvoskin B, Mathias M, Friedman M (2001) Infection of Acanthamoeba polyphaga with Simkania negevensis and S. negevensis survival within amoebal cysts. Appl Environ Microbiol 67:4789–4795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Khan N (2009) Acanthamoeba, biology and pathogenesis. Caister Academic Press, Norfolk

    Google Scholar 

  • Khan N, Panjwani N (2000) Pathogenesis of Acanthamoeba infections; conference booklet VIII European Multicolloquium of Parasitology; Poznan, Poland

  • King C, Shotts E, Wooley R, Porter K (1988) Survival of coliforms and bacterial pathogens within protozoa during chlorination. Appl Environ Microbiol 54:3023–3033

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleinig H, Sitte P (1984) Zellbiologie. Gustav Fischer, Stuttgart

    Google Scholar 

  • Krishna-Prasad B, Gupta S (1978) Preliminary report on engulfment and retention of mycobacteria by trophozoites of axenically grown Acanthamoeba castellanii Douglas. Curr Sci 47:245–247

    Google Scholar 

  • Kurek R, Scheid P, Michel R (2010) Darstellung von pilzartigen Endoparasiten bei freilebenden Amöben nach spezifischer Fluoreszenzanfärbung. Mikrokosmos 99(6):327–330

    Google Scholar 

  • La Scola B, Raoult D (1999) Afipia felis in hospital water supply in association with free-living amoebae. Lancet 353:1330

    Article  PubMed  Google Scholar 

  • La Scola B, Raoult D (2001) Survival of Coxiella burnetii within free-living amoeba Acanthamoeba castellanii. Clin Microbiol Infect 7:75–79

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Landers P, Kerr K, Rowbotham T, Tipper J, Keig P, Ingham E, Denton M (2000) Survival and growth of Burkholderia cepacia within the free-living amoeba Acanthamoeba polyphaga. Eur J Clin Microbiol Infect Dis 19:121–123

    Article  CAS  PubMed  Google Scholar 

  • Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, Lescot M, Poirot O, Bertaux L, Bruley C, Coute Y, Rivkina E, Abergel C, Claverie J-P (2014) Thirty-thousand-year-old distinct relative of ginat icosahedral DNA viruses with a pandoravirus morphology. PNAS 2014: published ahead of print; March 3

  • Ly T, Müller H (1990) Interactions of Listeria monocytogenes, Listeria seeligeri and Listeria innocua with protozoans. J Gen Appl Microbiol 36:143–150

    Article  Google Scholar 

  • Marciano-Cabral F, Cabral G (2007) The immune response to Naegleria fowleri amebae and pathogenesis of infection. FEMS Immunol Med Microbiol 51:243–259

    Article  CAS  PubMed  Google Scholar 

  • Michel R (1997) Freilebende Amöben als Wirte und Vehikel von Mikroorganismen. Mitt Österr Ges Tropenmed Parasitol 19:11–20

    Google Scholar 

  • Michel R, Wylezich C (2005) Beitrag zur Biologie und Morphologie von Cochlonema euryblastum, einem endoparasitischen Pilz von Thecamoeba quadrilineata. Mikrokosmos 94:75–79

    Google Scholar 

  • Michel R, Hauröder-Philippczyk B, Müller K-D, Weishaar I (1994) Acanthamoeba from human nasal mucosa infected with an obligate intracellular parasite. Eur J Protistol 30:104–110

    Article  Google Scholar 

  • Michel R, Müller K-D, Schmid E (1995) Ehrlichia-like organismus (KSL1) observed as obligate intracellular parasites of Saccamoeba species. Endocyt Cell Res 11:69–80

    Google Scholar 

  • Michel R, Müller K-D, Schmid E (1998) Legionella-like slender rods multiplying within a strain of Acanthamoeba sp. isolated from drinking water. Parasitol Res 84:84–88

    Article  CAS  PubMed  Google Scholar 

  • Michel R, Müller K-D, Hoffmann R (2001) Enlarged Chlamydia-like organisms as spontaneous infection of Acanthamoeba castellanii. Parasitol Res 87:248–251

    Article  CAS  PubMed  Google Scholar 

  • Michel R, Steinert M, Zöller L, Hauröder B, Henning K (2004) Cocultivation of protozoa and the Chlamydia-like bacterium Waddlia chondrophila isolated from an aborted bovine foetus in Germany. Acta Protozool 43:37–42

    Google Scholar 

  • Michel R, Müller K-D, Zöller L, Walochnik J, Hartmann M, Schmid E (2005) Free living amoebae serve as host for the Chlamydia-like bacterium Simkania nevegensis. Acta Protozool 44:113–121

    Google Scholar 

  • Molmeret M, Horn M, Wagner M, Santic M, Kwaik Y (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71:20–28

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rogers J, Keevil C (1992) Immunogold and fluorescein immunolabelling of Legionella pneumophila within an aquatic biofilm visualized by using episcopic differential interference contrast microscopy. Appl Environ Microbiol 58:2326–2330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rowbotham T (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33:1179–1183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Scheid PL, Schwarzenberger R (2011) Free-living amoebae as vectors of Cryptosporidia. Parasitol Res 109:499–504

    Article  PubMed  Google Scholar 

  • Scheid P, Schwarzenberger R (2012) Acanthamoeba spp. as vehicle and reservoir of adenoviruses. Parasitol Res. doi:10.1007/s00436-012-2828-7

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Scheid P, Hauröder B, Michel R (2010) Investigations of an extraordinary endocytobiont in Acanthamoeba sp.: development and replication. Parasitol Res 106:1371–1377

    Article  PubMed  Google Scholar 

  • Schimper A (1883) Über die Entwicklung der Chlorophyllkörner und Farbkörper. Bot Z 41:102–113

    Google Scholar 

  • Schwemmler W (1991) Symbiogenese als Motor der Evolution. Paul Parey, Berlin

    Google Scholar 

  • Siddiqui K, Khan N (2012) Biology and pathogenesis of Acanthamoeba. Parasit Vectors 5:6

    Article  PubMed Central  PubMed  Google Scholar 

  • Snelling W, McKenna J, Lecky D, Dooley J (2005) Survival of Campylobacter jejuni in waterborne protozoa. Appl Environ Microbiol 71:5560–5571

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Steenbergen J, Shuman H, Casadervall A (2001) Cryptococcus neoformans interactions with amoebae suggest an explanation for its violence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A 98:15245–15250

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Steinert M, Birkness K, White E, Fields B, Quinn F (1998) Mycobacterium avium bacilli grow saprozoically in coculture with Acanthamoeba polyphaga and survive within cyst walls. Appl Environ Microbiol 64:2256–2261

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tezcan-Merdol D, Ljungström M, Winiecka-Krusnell J, Linder E, Engstrand L, Rhen M (2004) Uptake and replication of Salmonella enterica in Acanthamoeba rhysodes. Appl Environ Microbiol 70:3706–3714

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thom S, Warhurst D, Drasar B (1992) Association of Vibrio cholerae with fresh water amoebae. J Med Microbiol 36:303–306

    Article  CAS  PubMed  Google Scholar 

  • Thomas V, Loret J, Jousset M, Greub G (2008) Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 10:2728–2745

    Article  CAS  PubMed  Google Scholar 

  • Tomov A, Tsvetkova E, Tomova I, Michailova L, Kassovski V (1999) Persistence and multiplication of obligate anaerobe bacteria in amoebae under aerobic conditions. Anaerobe 5:19–23

    Article  CAS  PubMed  Google Scholar 

  • Wagner Y, Noack B, Hoffmann T, Jacobs E, Lück P (2006) Periodontopathogenic bacteria multiply in the environmental amoeba Acanthamoeba castellani. Int J Hyg Environ Health 209:535–539

    Article  PubMed  Google Scholar 

  • Walochnik J, Aspöck H (2007) Amöben: Paradebeispiele für Probleme der Phylogenetik, Klassifikation und Nomenklatur. Denisia 20:323–350

    Google Scholar 

  • Wieser A, Schubert S (2011) Intra-und extrazelluläre Biofilme uropathogener E. coli. Chemother J 20:181–185

    Google Scholar 

  • Winiecka-Krusnell J, Wreiber K, von Euler A, Engstrand L, Linder E (2002) Free-living amoebae promote growth and survival of Helicobacter pylori. Scand J Infect Dis 34:253–256

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The author would like to thank Dr. David Lam (MD, MPH, Shaman Medical Consulting) for review and English-language editing of the article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick Scheid.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scheid, P. Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res 113, 2407–2414 (2014). https://doi.org/10.1007/s00436-014-3932-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-3932-7

Keywords

Navigation