Abstract
BackgroundThe gram-positive pathogenic bacterium Listeria monocytogenes is widely spread in the nature. L. monocytogenes was reported to be isolated from soil, water, sewage and sludge. Listeriolysin O (LLO) is a L. monocytogenes major virulence factor. In the course of infection in mammals, LLO is required for intracellular survival and apoptosis induction in lymphocytes. In this study, we explored the potential of LLO to promote interactions between L. monocytogenes and the ubiquitous inhabitant of natural ecosystems bacteriovorous free-living ciliate Tetrahymena pyriformis.ResultsWild type L. monocytogenes reduced T. pyriformis trophozoite counts and stimulated encystment. The effects were observed starting from 48 h of co-incubation. On the day 14, trophozoites were eliminated from the co-culture while about 5 × 104 cells/ml remained in the axenic T. pyriformis culture. The deficient in the LLO-encoding hly gene L. monocytogenes strain failed to cause mortality among protozoa and to trigger protozoan encystment. Replenishment of the hly gene in the mutant strain restored toxicity towards protozoa and induction of protozoan encystment. The saprophytic non-haemolytic species L. innocua transformed with the LLO-expressing plasmid caused extensive mortality and encystment in ciliates. During the first week of co-incubation, LLO-producing L. monocytogenes demonstrated higher growth rates in association with T. pyriformis than the LLO-deficient isogenic strain. At latter stages of co-incubation bacterial counts were similar for both strains. T. pyriformis cysts infected with wild type L. monocytogenes caused listerial infection in guinea pigs upon ocular and oral inoculation. The infection was proved by bacterial plating from the internal organs.ConclusionsThe L. monocytogenes virulence factor LLO promotes bacterial survival and growth in the presence of bacteriovorous ciliate T. pyriformis. LLO is responsible for L. monocytogenes toxicity for protozoa and induction of protozoan encystment. L. monocytogenes entrapped in cysts remained viable and virulent. In whole, LLO activity seems to support bacterial survival in the natural habitat outside of a host.
Highlights
Introduction of theListeriolysin O (LLO)-expressing plasmid produced a dramatic effect on the outcome of interactions between L. innocua and T. pyriformis
The gram-positive pathogenic bacterium Listeria monocytogenes is a causative agent of listeriosis, a food-borne disease associated with such severe manifestations as meningitis, meningoencephalitis and miscarriages in
We examined the involvement of LLO in the interactions of L. monocytogenes and the ciliate Tetrahymena pyriformis
Summary
Introduction of theLLO-expressing plasmid produced a dramatic effect on the outcome of interactions between L. innocua and T. pyriformis. LLO-expressing L. innocua accelerated T. pyriformis encystment as it was previously observed with L. monocytogenes. At 48 h cyst concentration was about 7 fold higher in the presence of LLO-expressing L. innocua compared to the wild type strain. The cyst concentration diminished by a factor 5.6 between 48 h and 72 h, the effect was not observed in the presence of wild type L. monocytogenes. The gram-positive pathogenic bacterium Listeria monocytogenes is widely spread in the nature. L. monocytogenes was reported to be isolated from soil, water, sewage and sludge. We explored the potential of LLO to promote interactions between L. monocytogenes and the ubiquitous inhabitant of natural ecosystems bacteriovorous freeliving ciliate Tetrahymena pyriformis. Being ubiquitously distributed in the environment, L. monocytogenes may be involved in the interactions with free-living protozoa, a common representative of natural ecosystems. Besides its role in pathogen’s intracellular replication, LLO can cause apoptosis in dendritic cells and lymphocytes during first days of infection in mice [17,18]
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