Abstract
Listeria monocytogenes is a foodborne opportunistic pathogen capable to switch from an environmental saprophyte to a potentially fatal human pathogen. The fact that the pathogen maintains the genes suitable for an elaborate infectious process indicates that these genes are required to survive in the environment. However, no environmental host reservoir for L. monocytogenes has been identified so far. The similarity of free-living, bacteria-scavenging amoebae to macrophages led to the hypothesis that protozoa may represent the missing link in the ecology and pathology of L. monocytogenes. Consequently, numerous studies have been published reporting on the potential of Acanthamoeba spp. to serve as host for a variety of pathogenic bacteria. However, the data on the interaction of L. monocytogenes with Acanthamoeba spp. are inconsistent and relatively little information on the impact of this interaction on growth and distribution of the foodborne pathogen is currently available. Hence, this review focuses on the interaction of L. monocytogenes and Acanthamoeba spp. affecting survival and growth of the foodborne pathogen in natural and man-made environments, in order to highlight the potential impact of this interplay on food safety and human health.

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Abd H, Johansson T, Golovliov I, Sandstrom G, Forsman M (2003) Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microbiol 69:600–606
Abd H, Saeed A, Weintraub A, Nair GB, Sandstrom G (2007) Vibrio cholerae O1 strains are facultative intracellular bacteria, able to survive and multiply symbiotically inside the aquatic free-living amoeba Acanthamoeba castellanii. FEMS Microbiol Ecol 60:33–39. doi:10.1111/j.1574-6941.2006.00254.x
Akya A, Pointon A, Thomas C (2009a) Mechanism involved in phagocytosis and killing of Listeria monocytogenes by Acanthamoeba polyphaga. Parasitol Res 105:1375–1383. doi:10.1007/s00436-009-1565-z
Akya A, Pointon A, Thomas C (2009b) Viability of Listeria monocytogenes in co-culture with Acanthamoeba spp. FEMS Microbiol Ecol 70:20–29. doi:10.1111/j.1574-6941.2009.00736.x
Akya A, Pointon A, Thomas C (2010) Listeria monocytogenes does not survive ingestion by Acanthamoeba polyphaga. Microbiology 156:809–818. doi:10.1099/mic.0.031146-0
Alsam S, Sissons J, Dudley R, Khan NA (2005) Mechanisms associated with Acanthamoeba castellanii (T4) phagocytosis. Parasitol Res 96:402–409. doi:10.1007/s00436-005-1401-z
Amann R, Springer N, Schönhuber W, Ludwig W, Schmid EN, Müller KD, Michel R (1997) Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl Environ Microbiol 63:115–121
Anacarso I, de Niederhäusern S, Messi P, Guerrieri E, Iseppi R, Sabia C, Bondi M (2012) Acanthamoeba polyphaga, a potential environmental vector for the transmission of food-borne and opportunistic pathogens. J Basic Microbiol 52:261–268. doi:10.1002/jobm.201100097
Arhets P, Gounon P, Sansonetti P, Guillen N (1995) Myosin II is involved in capping and uroid formation in the human pathogen Entamoeba histolytica. Infect Immun 63:4358–4367
Band RN, Mohrlok S (1973) The cell cycle and induced amitosis in Acanthamoeba. J Protozool 20:654–657
Berrang ME, Meinersmann RJ, Frank JF, Ladely SR (2010) Colonization of a newly constructed commercial chicken further processing plant with Listeria monocytogenes. J Food Prot 73:286–291
Birtles RJ, Rowbotham TJ, Raoult D, Harrison TG (1996) Phylogenetic diversity of intra-amoebal legionellae as revealed by 16S rRNA gene sequence comparison. Microbiology 142(Pt 12):3525–3530
Bonazzi M, Lecuit M, Cossart P (2009) Listeria monocytogenes internalin and E-cadherin: from bench to bedside. Cold Spring Harb Perspect Biol 1:a003087. doi:10.1101/cshperspect.a003087
Bowers B, Korn ED (1973) Cytochemical identification of phosphatase activity in the contractile vacuole of Acanthamoeba castellanii. J Cell Biol 59:784–791
Bozue JA, Johnson W (1996) Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome–lysosome fusion. Infect Immun 64:668–673
Brandl MT, Rosenthal BM, Haxo AF, Berk SG (2005) Enhanced survival of Salmonella enterica in vesicles released by a soilborne Tetrahymena species. Appl Environ Microbiol 71:1562–1569. doi:10.1128/AEM.71.3.1562-1569.2005
Brock DA, Douglas TE, Queller DC, Strassmann JE (2011) Primitive agriculture in a social amoeba. Nature 469:393–396. doi:10.1038/nature09668
Brown MR, Barker J (1999) Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol 7:46–50
Cirillo JD (1999) Exploring a novel perspective on pathogenic relationships. Trends Microbiol 7:96–98
Doyscher D, Fieseler L, Dons L, Loessner MJ, Schuppler M (2013) Acanthamoeba feature a unique backpacking strategy to trap and feed on Listeria monocytogenes and other motile bacteria. Environ Microbiol 15:433–446. doi:10.1111/j.1462-2920.2012.02858.x
Essig A, Heinemann M, Simnacher U, Marre R (1997) Infection of Acanthamoeba castellanii by Chlamydia pneumoniae. Appl Environ Microbiol 63:1396–1399
Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55:476–511
Fenlon DR (1985) Wild birds and silage as reservoirs of Listeria in the agricultural environment. J Appl Bacteriol 59:537–543
Fenlon DR (1999) Listeria monocytogenes in the natural environment. In: Ryser ET, Marth EH (eds) Listeria, listeriosis, and food safety. CRC Press, Boca Raton, pp 21–37
Fenlon DR, Stewart T, Donachie W (1995) The incidence, numbers and types of Listeria monocytogenes isolated from farm bulk tank milks. Lett Appl Microbiol 20:57–60
Fenlon DR, Wilson J, Donachie W (1996) The incidence and level of Listeria monocytogenes contamination of food sources at primary production and initial processing. J Appl Bacteriol 81:641–650
Fields BS, Fields SR, Loy JN, White EH, Steffens WL, Shotts EB (1993) Attachment and entry of Legionella pneumophila in Hartmannella vermiformis. J Infect Dis 167:1146–1150
Fieseler L, Doyscher D, Loessner ML, Schuppler M (2014) Acanthamoeba release compounds which promote growth of Listeria monocytogenes and other bacteria. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-5534-9.
Gasanov U, Hughes D, Hansbro PM (2005) Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiol Rev 29:851–875. doi:10.1016/j.femsre.2004.12.002
Gourabathini P, Brandl MT, Redding KS, Gunderson JH, Berk SG (2008) Interactions between food-borne pathogens and protozoa isolated from lettuce and spinach. Appl Environ Microbiol 74:2518–2525. doi:10.1128/AEM.02709-07
Greub G, Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17:413–433
Hagedorn M, Rohde KH, Russell DG, Soldati T (2009) Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323:1729–1733. doi:10.1126/science.1169381
Holden EP, Winkler HH, Wood DO, Leinbach ED (1984) Intracellular growth of Legionella pneumophila within Acanthamoeba castellanii Neff. Infect Immun 45:18–24
Huws SA, Morley RJ, Jones MV, Brown MR, Smith AW (2008) Interactions of some common pathogenic bacteria with Acanthamoeba polyphaga. FEMS Microbiol Lett 282:258–265. doi:10.1111/j.1574-6968.2008.01123.x
Janda WM (2010) Amoeba-resistant bacteria: their role in human infections. Clin Microbiol Newsl 32:177–184
Kilvington S, Price J (1990) Survival of Legionella pneumophila within cysts of Acanthamoeba polyphaga following chlorine exposure. J Appl Bacteriol 68:519–525
Kress H, Stelzer EH, Holzer D, Buss F, Griffiths G, Rohrbach A (2007) Filopodia act as phagocytic tentacles and pull with discrete steps and a load-dependent velocity. Proc Natl Acad Sci U S A 104:11633–11638. doi:10.1073/pnas.0702449104
Kushwaha K, Muriana PM (2009) Adherence characteristics of Listeria strains isolated from three ready-to-eat meat processing plants. J Food Prot 72:2125–2131
La Scola B, Raoult D (2001) Survival of Coxiella burnetii within free-living amoeba Acanthamoeba castellanii. Clin Microbiol Infect 7:75–79
Ly TM, Muller HE (1990) Ingested Listeria monocytogenes survive and multiply in protozoa. J Med Microbiol 33:51–54
MacGowan AP, Bowker K, McLauchlin J, Bennett PM, Reeves DS (1994) The occurrence and seasonal changes in the isolation of Listeria spp. in shop bought food stuffs, human faeces, sewage and soil from urban sources. Int J Food Microbiol 21:325–334
Marciano-Cabral F, Cabral G (2003) Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev 16:273–307
Matz C, Jurgens K (2005) High motility reduces grazing mortality of planktonic bacteria. Appl Environ Microbiol 71:921–929. doi:10.1128/AEM.71.2.921-929.2005
Matz C, Kjelleberg S (2005) Off the hook—how bacteria survive protozoan grazing. Trends Microbiol 13:302–307. doi:10.1016/j.tim.2005.05.009
Miettinen H, Wirtanen G (2005) Prevalence and location of Listeria monocytogenes in farmed rainbow trout. Int J Food Microbiol 104:135–143. doi:10.1016/j.ijfoodmicro.2005.01.013
Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl Environ Microbiol 71:20–28. doi:10.1128/AEM.71.1.20-28.2005
Nightingale KK, Schukken YH, Nightingale CR, Fortes ED, Ho AJ, Her Z, Grohn YT, McDonough PL, Wiedmann M (2004) Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Appl Environ Microbiol 70:4458–4467. doi:10.1128/AEM.70.8.4458-4467.2004
Oliver HF, Wiedmann M, Boor KJ (2007) Environmental reservoir and transmission into the mammalian host. In: Goldfine H, Shen H (eds) Listeria monocytogenes: pathogenesis and host response. Springer (US), New York, pp 111–137
Pingulkar K, Kamat A, Bongirwar D (2001) Microbiological quality of fresh leafy vegetables, salad components and ready-to-eat salads: an evidence of inhibition of Listeria monocytogenes in tomatoes. Int J Food Sci Nutr 52:15–23
Pollard TD, Shelton E, Weihing RR, Korn ED (1970) Ultrastructural characterization of F-actin isolated from Acanthamoeba castellanii and identification of cytoplasmic filaments as F-actin by reaction with rabbit heavy meromyosin. J Mol Biol 50:91–97
Preston TM, Richards H, Wotton RS (2001) Locomotion and feeding of Acanthamoeba at the water–air interface of ponds. FEMS Microbiol Lett 194:143–147
Pushkareva VI, Ermolaeva SA (2010) Listeria monocytogenes virulence factor Listeriolysin O favors bacterial growth in co-culture with the ciliate Tetrahymena pyriformis, causes protozoan encystment and promotes bacterial survival inside cysts. BMC Microbiol 10:26. doi:10.1186/1471-2180-10-26
Roberts AJ, Wiedmann M (2003) Pathogen, host and environmental factors contributing to the pathogenesis of listeriosis. Cell Mol Life Sci 60:904–918. doi:10.1007/s00018-003-2225-6
Romero S, Grompone G, Carayol N, Mounier J, Guadagnini S, Prevost MC, Sansonetti PJ, Van Nhieu GT (2011) ATP-mediated Erk1/2 activation stimulates bacterial capture by filopodia, which precedes Shigella invasion of epithelial cells. Cell Host Microbe 9:508–519. doi:10.1016/j.chom.2011.05.005
Rorvik LM, Aase B, Alvestad T, Caugant DA (2003) Molecular epidemiological survey of Listeria monocytogenes in broilers and poultry products. J Appl Microbiol 94:633–640
Rude RA, Jackson GJ, Bier JW, Sawyer TK, Risty NG (1984) Survey of fresh vegetables for nematodes, amoebae, and Salmonella. J Assoc Off Anal Chem 67:613–615
Sandstrom G, Saeed A, Abd H (2010) Acanthamoeba polyphaga is a possible host for Vibrio cholerae in aquatic environments. Exp Parasitol 126:65–68. doi:10.1016/j.exppara.2009.09.021
Sauders BD, Wiedmann M (2007) Ecology of Listeria species and L. monocytogenes in the natural environment. In: Ryser ET, Marth EH (eds) Listeria, listeriosis, and food safety, 3rd edn. CRC Press, Boca Raton, pp 21–54
Schlech WF 3rd, Lavigne PM, Bortolussi RA, Allen AC, Haldane EV, Wort AJ, Hightower AW, Johnson SE, King SH, Nicholls ES (1983) Epidemic listeriosis—evidence for transmission by food. N Engl J Med 308:203–206. doi:10.1056/NEJM198301273080407
Schuchat A, Deaver KA, Wenger JD, Plikaytis BD, Mascola L, Pinner RW, Reingold AL, Broome CV (1992) Role of foods in sporadic listeriosis: I. Case-control study of dietary risk factors. The Listeria Study Group. JAMA 267:2041–2045
Schuppler M, Loessner MJ (2010) The opportunistic pathogen Listeria monocytogenes: pathogenicity and interaction with the mucosal immune system. Int J Inflamm 2010:704321. doi:10.4061/2010/704321
Siddiqui R, Khan NA (2012) Biology and pathogenesis of Acanthamoeba. Parasit Vectors 5:6. doi:10.1186/1756-3305-5-6
Sinclair JL, McClellan JF, Coleman DC (1981) Nitrogen mineralization by Acanthamoeba polyphaga in grazed Pseudomonas paucimobilis populations. Appl Environ Microbiol 42:667–671
Steenbergen JN, Shuman HA, Casadevall A (2001) Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A 98:15245–15250. doi:10.1073/pnas.261418798
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
Tezcan-Merdol D, Ljungstrom 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. doi:10.1128/AEM.70.6.3706-3714.2004
Vaerewijck MJ, Sabbe K, Bare J, Houf K (2008) Microscopic and molecular studies of the diversity of free-living protozoa in meat-cutting plants. Appl Environ Microbiol 74:5741–5749. doi:10.1128/AEM.00980-08
Vaerewijck MJ, Sabbe K, Bare J, Houf K (2011) Occurrence and diversity of free-living protozoa on butterhead lettuce. Int J Food Microbiol 147:105–111. doi:10.1016/j.ijfoodmicro.2011.03.015
Vaerewijck MJ, Sabbe K, Van Hende J, Bare J, Houf K (2010) Sampling strategy, occurrence and diversity of free-living protozoa in domestic refrigerators. J Appl Microbiol 109:1566–1578. doi:10.1111/j.1365-2672.2010.04783.x
Wagner Y, Noack B, Hoffmann T, Jacobs E, Christian Luck P (2006) Periodontopathogenic bacteria multiply in the environmental amoeba Acanthamoeba castellani. Int J Hyg Environ Health 209:535–539. doi:10.1016/j.ijheh.2006.05.006
Weber A, Potel J, Schafer-Schmidt R (1995a) The occurrence of Listeria monocytogenes in fecal samples of pigeons. Berl Munch Tierarztl Wochenschr 108:26–27
Weber A, Potel J, Schafer-Schmidt R, Prell A, Datzmann C (1995b) Studies on the occurrence of Listeria monocytogenes in fecal samples of domestic and companion animals. Zentralbl Hyg Umweltmed 198:117–123
Yokoyama E, Saitoh T, Maruyama S, Katsube Y (2005) The marked increase of Listeria monocytogenes isolation from contents of swine cecum. Comp Immunol Microbiol Infect Dis 28:259–268. doi:10.1016/j.cimid.2005.03.002
Zhou X, Elmose J, Call DR (2007) Interactions between the environmental pathogen Listeria monocytogenes and a free-living protozoan (Acanthamoeba castellanii). Environ Microbiol 9:913–922. doi:10.1111/j.1462-2920.2006.01213.x
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Schuppler, M. How the interaction of Listeria monocytogenes and Acanthamoeba spp. affects growth and distribution of the food borne pathogen. Appl Microbiol Biotechnol 98, 2907–2916 (2014). https://doi.org/10.1007/s00253-014-5546-5
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DOI: https://doi.org/10.1007/s00253-014-5546-5


