Abstract
It is generally accepted that selection for resistance to grazing by protists has contributed to the evolution of Legionella pneumophila as a pathogen. Grazing resistance is becoming more generally recognized as having an important role in the ecology and evolution of bacterial pathogenesis. However, selection for grazing resistance presupposes the existence of protist grazers that provide the selective pressure. To determine whether there are protists that graze on pathogenic Legionella species, we investigated the existence of such organisms in a variety of environmental samples. We isolated and characterized diverse protists that graze on L. pneumophila and determined the effects of adding L. pneumophila on the protist community structures in microcosms made from these environmental samples. Several unrelated organisms were able to graze efficiently on L. pneumophila. The community structures of all samples were markedly altered by the addition of L. pneumophila. Surprisingly, some of the Legionella grazers were closely related to species that are known hosts for L. pneumophila, indicating the presence of unknown specificity determinants for this interaction. These results provide the first direct support for the hypothesis that protist grazers exert selective pressure on Legionella to acquire and retain adaptations that contribute to survival, and that these properties are relevant to the ability of the bacteria to cause disease in people. We also report a novel mechanism of killing of amoebae by one Legionella species that requires an intact Type IV secretion system but does not involve intracellular replication. We refer to this phenomenon as ‘food poisoning’.
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Acknowledgements
This work was supported by an award from NIAID, 5RO1AI23549 (H.A.S.) and funds from the Department of Microbiology, University of Chicago. F Amaro was supported by a postdoctoral fellowship from the Fulbright Commission and Ministry of Education of Spain. We thank our colleagues for supplying samples of various Legionella species, including Barry Fields and Claressa Lucas at CDC and Paul Edelstein at the University of Pennsylvania. We would like to thank the following individuals for supplying environmental samples used in this work: Dr Juan Carlos Gutiérrez from the Department of Microbiology III, Complutense University of Madrid, Dr Maureen Coleman from the Department of Geophysics at the University of Chicago and Dr Geeta K Rijal from the Metropolitan Water Reclamation District of Greater Chicago. The authors would like to express their appreciation to the Integrated Ocean Drilling Program shipboard technical, operations and engineering personnel of Integrated Ocean Drilling Program Expedition 311 for collecting, archiving and providing the ocean subsurface sample used in this research. Funding for Integrated Ocean Drilling Program was provided by the following agencies at the time of this expedition: European Consortium for Ocean Research Drilling, Ministry of Education, Culture, Sports, Science and Technology of Japan. Ministry of Science and Technology, People’s Republic of China, National Science Foundation (United States). Any opinions, findings and conclusions or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the participating agencies, Integrated Ocean Drilling Program Management International or the Integrated Ocean Drilling Program Implementing Organizations. This is Lamont–Doherty Contribution No. 7850.
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Amaro, F., Wang, W., Gilbert, J. et al. Diverse protist grazers select for virulence-related traits in Legionella. ISME J 9, 1607–1618 (2015). https://doi.org/10.1038/ismej.2014.248
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DOI: https://doi.org/10.1038/ismej.2014.248
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