Abstract
The susceptibility of coliform bacteria and bacterial pathogens to free chlorine residuals was determined before and after incubation with amoebae and ciliate protozoa. Viability of bacteria was quantified to determine their resistance to free chlorine residuals when ingested by laboratory strains of Acanthamoeba castellanii and Tetrahymena pyriformis. Cocultures of bacteria and protozoa were incubated to facilitate ingestion of the bacteria and then were chlorinated, neutralized, and sonicated to release intracellular bacteria. Qualitative susceptibility of protozoan strains to free chlorine was also assessed. Protozoa were shown to survive and grow after exposure to levels of free chlorine residuals that killed free-living bacteria. Ingested coliforms Escherichia coli, Citrobacter freundii, Enterobacter agglomerans, Enterobacter cloacae, Klebsiella pneumoniae, and Klebsiella oxytoca and bacterial pathogens Salmonella typhimurium, Yersinia enterocolitica, Shigella sonnei, Legionella gormanii, and Campylobacter jejuni had increased resistance to free chlorine residuals. Bacteria could be cultured from within treated protozoans well after the time required for 99% inactivation of free-living cells. All bacterial pathogens were greater than 50-fold more resistant to free chlorine when ingested by T. pyriformis. Escherichia coli ingested by a Cyclidium sp., a ciliate isolated from a drinking water reservoir, were also shown to be more resistant to free chlorine. The mechanism that increased resistance appeared to be survival within protozoan cells. This study indicates that bacteria can survive ingestion by protozoa. This bacterium-protozoan association provides bacteria with increased resistance to free chlorine residuals which can lead to persistence of bacteria in chlorine-treated water. We propose that resistance to digestion by predatory protozoa was an evolutionary precursor of pathogenicity in bacteria and that today it is a mechanism for survival of fastidious bacteria in dilute and inhospitable aquatic environments.
MeSH Terms
Animals
Bacteria/drug effects,pathogenicity,ultrastructure
Chlorine/pharmacology
Drug Resistance, Microbial
Enterobacteriaceae/drug effects
Eukaryota/drug effects,microbiology,ultrastructure
Microscopy, Electron
Virulence
Water Microbiology
Water Supply
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
King C H
Department of Medical Microbiology, College of Veterinary Medicine, Athens, Georgia.
Shotts E B
Wooley R E
Porter K G
References (31)
31 references, click to expand
-
Ultrastructural evidence for the presence of bacteria, viral-like particles, and mycoplasma-like organisms associated with Giardia spp.
J Protozool. 1988 Feb;35(1):151-8
PMID: 3284999
-
Transmission electron microscopy of tissue prepared for scanning electron microscopy by ethanol-cryofracturing.
Stain Technol. 1975 Mar;50(2):119-25
PMID: 1145653
-
Differences in destruction of cysts of pathogenic and nonpathogenic Naegleria and Acanthamoeba by chlorine.
Appl Environ Microbiol. 1976 Feb;31(2):294-7
PMID: 999278
-
Injured coliforms in drinking water.
Appl Environ Microbiol. 1986 Jan;51(1):1-5
PMID: 3513698
-
Rates of digestion of bacteria by marine phagotrophic protozoa: temperature dependence.
Appl Environ Microbiol. 1988 May;54(5):1091-5
PMID: 16347623
-
Kappa and other endosymbionts in Paramecium aurelia.
Bacteriol Rev. 1974 Jun;38(2):113-63
PMID: 4599970
-
[Free-living Amoebae in fresh water. Study of the water supply of the town of Poitiers (France) (author's transl)].
Bull Soc Pathol Exot Filiales. 1981 Sep-Oct;74(5):521-4
PMID: 7318052
-
Investigation and control of an outbreaks of legionnaires' disease in a district general hospital.
Lancet. 1981 Apr 25;1(8226):932-6
PMID: 6112337
-
A low-viscosity epoxy resin embedding medium for electron microscopy.
J Ultrastruct Res. 1969 Jan;26(1):31-43
PMID: 4887011
-
Factors promoting survival of bacteria in chlorinated water supplies.
Appl Environ Microbiol. 1988 Mar;54(3):649-54
PMID: 3288119
-
Ecology of Legionella pneumophila within water distribution systems.
Appl Environ Microbiol. 1985 Jan;49(1):221-8
PMID: 3977311
-
Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyriformis.
Appl Environ Microbiol. 1984 Mar;47(3):467-71
PMID: 6424568
-
Survival strategies of bacteria in the natural environment.
Microbiol Rev. 1987 Sep;51(3):365-79
PMID: 3312987
-
Electron microscopic studies of Acanthamoeba castellanii infected with obligate intracellular bacterial parasite.
Acta Microbiol Pol. 1979;28(2):123-33
PMID: 89791
-
Chlorine resistance patterns of bacteria from two drinking water distribution systems.
Appl Environ Microbiol. 1982 Oct;44(4):972-87
PMID: 7149722
-
Survival and multiplication of Legionella pneumophila in municipal drinking water systems.
Appl Environ Microbiol. 1987 May;53(5):979-86
PMID: 3606101
-
Enumeration of indicator bacteria exposed to chlorine.
Adv Appl Microbiol. 1983;29:177-93
PMID: 6650262
-
Enhanced chlorine resistance of tap water-adapted Legionella pneumophila as compared with agar medium-passaged strains.
Appl Environ Microbiol. 1985 Jul;50(1):21-6
PMID: 3896142
-
Selection of antibiotic-resistant standard plate count bacteria during water treatment.
Appl Environ Microbiol. 1982 Aug;44(2):308-16
PMID: 7125650
-
Edrophonium-induced inward membrane current in single neurons physically isolated from Aplysia californica.
Brain Res. 1988 Jan 12;438(1-2):95-100
PMID: 3345453
-
Activity and distribution of bacteriolytic N-acetyl-muramidase during growth of Acanthamoeba castellanii in axenic culture.
Acta Microbiol Pol. 1978;27(3):243-56
PMID: 81598
-
Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila.
Appl Environ Microbiol. 1986 Feb;51(2):422-4
PMID: 3954351
-
Infections of Paramecium bursaria with bacteria and yeasts.
J Cell Sci. 1982 Dec;58:445-53
PMID: 7183698
-
Waterborne giardiasis in the United States: a review.
Am J Public Health. 1979 Aug;69(8):817-9
PMID: 453418
-
Survival, and protection against chlorination, of human enteric pathogens in free-living nematodes isolated from water supplies.
Am J Trop Med Hyg. 1960 Mar;9:136-42
PMID: 13809161
-
An ultrastructural study of ingestion and digestion in Tetrahymena pyriformis.
J Protozool. 1966 May;13(2):311-23
PMID: 5953849
-
Pathogenic and nonpathogenic Acanthamoeba spp. in thermally polluted discharges and surface waters.
J Protozool. 1981 Feb;28(1):56-9
PMID: 7252886
-
Comparison of guinea pig and protozoan models for determining virulence of Legionella species.
Infect Immun. 1986 Sep;53(3):553-9
PMID: 3744550
-
Feeding activity by Amoeba proteus.
Exp Cell Res. 1961 Sep;24:618-20
PMID: 14496464
-
Inactivation of Campylobacter jejuni by chlorine and monochloramine.
Appl Environ Microbiol. 1986 Feb;51(2):307-11
PMID: 3954344
-
Lysosomal physiology in Tetrahymena. 3. Pharmacological studies on acid hydrolase release and the ingestion and egestion of dimethylbenzanthracene particles.
J Cell Biol. 1974 Sep;62(3):844-59
PMID: 4152946