Persistence of Free-Living Protozoan Communities across Rearing Cycles in Commercial Poultry Houses

Baré, Julie; Houf, Kurt; Verstraete, Tine; Vaerewijck, Mario; Sabbe, Koen

doi:10.1128/aem.01756-10

Cited by 13 publications

(15 citation statements)

References 42 publications

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“…Likewise, pre-exposure to stress may affect the interaction of stressed C. jejuni cells with amoeba. To date, little is known about the interaction of stressed C. jejuni and A. castellanii , but this needs to be investigated as both of these organisms occupy a similar ecological habitat [21,31,32]. The importance of the interplay between C. jejuni and amoeba under stress conditions was recently highlighted by the fact that co-incubation with amoeba increases acid tolerance and survival of C. jejuni [24,26,27,33].…”

Section: Introductionmentioning

confidence: 99%

Effect of environmental stress factors on the uptake and survival of Campylobacter jejuni in Acanthamoeba castellanii

et al. 2012

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BackgroundCampylobacter jejuni is a major cause of bacterial food-borne illness in Europe and North America. The mechanisms allowing survival in the environment and transmission to new hosts are not well understood. Environmental free-living protozoa may facilitate both processes. Pre-exposure to heat, starvation, oxidative or osmotic stresses encountered in the environment may affect the subsequent interaction of C. jejuni with free-living protozoa. To test this hypothesis, we examined the impact of environmental stress on expression of virulence-associated genes (ciaB, dnaJ, and htrA) of C. jejuni and on its uptake by and intracellular survival within Acanthamoeba castellanii.ResultsHeat, starvation and osmotic stress reduced the survival of C. jejuni significantly, whereas oxidative stress had no effect. Quantitative RT-PCR experiments showed that the transcription of virulence genes was slightly up-regulated under heat and oxidative stresses but down-regulated under starvation and osmotic stresses, the htrA gene showing the largest down-regulation in response to osmotic stress. Pre-exposure of bacteria to low nutrient or osmotic stress reduced bacterial uptake by amoeba, but no effect of heat or oxidative stress was observed. Finally, C. jejuni rapidly lost viability within amoeba cells and pre-exposure to oxidative stress had no significant effect on intracellular survival. However, the numbers of intracellular bacteria recovered 5 h post-gentamicin treatment were lower with starved, heat treated or osmotically stressed bacteria than with control bacteria. Also, while ~1.5 × 103 colony forming unit/ml internalized bacteria could typically be recovered 24 h post-gentamicin treatment with control bacteria, no starved, heat treated or osmotically stressed bacteria could be recovered at this time point. Overall, pre-exposure of C. jejuni to environmental stresses did not promote intracellular survival in A. castellanii.ConclusionsTogether, these findings suggest that the stress response in C. jejuni and its interaction with A. castellanii are complex and multifactorial, but that pre-exposure to various stresses does not prime C. jejuni for survival within A. castellanii.

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Section: Introductionmentioning

confidence: 99%

Effect of environmental stress factors on the uptake and survival of Campylobacter jejuni in Acanthamoeba castellanii

et al. 2012

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“…Free-living protozoa are unicellular, heterotrophic, eukaryotic microorganisms ubiquitous in natural and anthropogenic aquatic and terrestrial environments, including food-related environments (10)(11)(12)(13). Free-living protozoa, including members of the amoebal genus Acanthamoeba, graze on bacteria and are therefore considered important bacterial predators.…”

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confidence: 99%

Behavior of Yersinia enterocolitica in the Presence of the Bacterivorous Acanthamoeba castellanii

Lambrecht

Baré

Damme

et al. 2013

Appl Environ Microbiol

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c Free-living protozoa play an important role in the ecology and epidemiology of human-pathogenic bacteria. In the present study, the interaction between Yersinia enterocolitica, an important food-borne pathogen, and the free-living amoeba Acanthamoeba castellanii was studied. Several cocultivation assays were set up to assess the resistance of Y. enterocolitica to A. castellanii predation and the impact of environmental factors and bacterial strain-specific characteristics. Results showed that all Y. enterocolitica strains persist in association with A. castellanii for at least 14 days, and associations with A. castellanii enhanced survival of Yersinia under nutrient-rich conditions at 25°C and under nutrient-poor conditions at 37°C. Amoebae cultivated in the supernatant of one Yersinia strain showed temperature-and time-dependent permeabilization. Intraprotozoan survival of Y. enterocolitica depended on nutrient availability and temperature, with up to 2.8 log CFU/ml bacteria displaying intracellular survival at 7°C for at least 4 days in nutrient-rich medium. Transmission electron microscopy was performed to locate the Yersinia cells inside the amoebae. As Yersinia and Acanthamoeba share similar ecological niches, this interaction identifies a role of free-living protozoa in the ecology and epidemiology of Y. enterocolitica.

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“…Indeed, despite strict hygiene management in commercial poultry houses, free-living protozoa, including T. pyriformis, are common and widespread throughout consecutive rearing cycles in both water and dry samples from such farms. Therefore, potential cross-contamination of bacterial pathogens, via free-living protozoa, between rearing cycles cannot be prevented (61,62). It could be expected that survival of C. jejuni in water systems, such as farm water distribution systems or slaughterhouse chillers, could be significantly increased by the presence of T. pyriformis.…”

Section: Discussionmentioning

confidence: 99%

Packaging of Campylobacter jejuni into Multilamellar Bodies by the Ciliate Tetrahymena pyriformis

Trigui

Paquet

Charette

et al. 2016

Appl Environ Microbiol

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dCampylobacter jejuni is the leading cause of bacterial gastroenteritis worldwide. Transmission to humans occurs through consumption of contaminated food or water. The conditions affecting the persistence of C. jejuni in the environment are poorly understood. Some protozoa package and excrete bacteria into multilamellar bodies (MLBs). Packaged bacteria are protected from deleterious conditions, which increases their survival. We hypothesized that C. jejuni could be packaged under aerobic conditions by the amoeba Acanthamoeba castellanii or the ciliate Tetrahymena pyriformis, both of which are able to package other pathogenic bacteria. A. castellanii did not produce MLBs containing C. jejuni. In contrast, when incubated with T. pyriformis, C. jejuni was ingested, packaged in MLBs, and then expelled into the milieu. The viability of the bacteria inside MLBs was confirmed by microscopic analyses. The kinetics of C. jejuni culturability showed that packaging increased the survival of C. jejuni up to 60 h, in contrast to the strong survival defect seen in ciliate-free culture. This study suggests that T. pyriformis may increase the risk of persistence of C. jejuni in the environment and its possible transmission between different reservoirs in food and potable water through packaging. Campylobacter jejuni is a leading cause of human gastroenteritis worldwide and a major public health problem (1-3). Severe symptoms of C. jejuni infection include high fever, watery to bloody diarrhea, nausea, and vomiting (4). In severe cases, C. jejuni is associated with serious postinfectious complications, such as Guillain-Barré syndrome (5, 6).Despite causing a serious disease in humans, C. jejuni is usually viewed as commensal in chickens (7) and livestock animals such as cattle (8) and pigs (9). Once these animals are colonized with Campylobacter spp., they excrete large numbers of the microorganisms in their feces and commonly contaminate different aquatic habitats, such as surface waters close to farming activities, agricultural runoff, wastewater effluent, sewage, and marine environments (10). Numerous epidemiological studies have demonstrated that water is not only a significant reservoir of C. jejuni but also an important factor for the spread of C. jejuni in farms, throughout flocks, and in slaughterhouses (11-15).C. jejuni requires a microaerobic environment (80% N 2 , 10% CO 2 , 5% H 2 , and 5% O 2 ) (16) and a narrow range of temperatures (37 to 43°C) for optimal growth (17). Because of the constraints imposed by its sensitivity to oxygen, C. jejuni is considered less able to tolerate environmental stress than other foodborne pathogens (18). Once outside the host, however, the interaction of C. jejuni with other microorganisms could help it survive high concentrations of oxygen and other environmental stresses.Since the study by Snelling et al. (19), in which Campylobacter and protozoa were isolated from the same broiler drinking water systems, the potential interactions between these microorganisms have been investigate...

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Persistence of Free-Living Protozoan Communities across Rearing Cycles in Commercial Poultry Houses

Cited by 13 publications

References 42 publications

Effect of environmental stress factors on the uptake and survival of Campylobacter jejuni in Acanthamoeba castellanii

Effect of environmental stress factors on the uptake and survival of Campylobacter jejuni in Acanthamoeba castellanii

Behavior of Yersinia enterocolitica in the Presence of the Bacterivorous Acanthamoeba castellanii

Packaging of Campylobacter jejuni into Multilamellar Bodies by the Ciliate Tetrahymena pyriformis

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