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      From Many Hosts, One Accidental Pathogen: The Diverse Protozoan Hosts of Legionella

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          Abstract

          The 1976 outbreak of Legionnaires' disease led to the discovery of the intracellular bacterial pathogen Legionella pneumophila. Given their impact on human health, Legionella species and the mechanisms responsible for their replication within host cells are often studied in alveolar macrophages, the primary human cell type associated with disease. Despite the potential severity of individual cases of disease, Legionella are not spread from person-to-person. Thus, from the pathogen's perspective, interactions with human cells are accidents of time and space—evolutionary dead ends with no impact on Legionella's long-term survival or pathogenic trajectory. To understand Legionella as a pathogen is to understand its interaction with its natural hosts: the polyphyletic protozoa, a group of unicellular eukaryotes with a staggering amount of evolutionary diversity. While much remains to be understood about these enigmatic hosts, we summarize the current state of knowledge concerning Legionella's natural host range, the diversity of Legionella-protozoa interactions, the factors influencing these interactions, the importance of avoiding the generalization of protozoan-bacterial interactions based on a limited number of model hosts and the central role of protozoa to the biology, evolution, and persistence of Legionella in the environment.

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          Most cited references132

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          Legionella and Legionnaires' disease: 25 years of investigation.

          There is still a low level of clinical awareness regarding Legionnaires' disease 25 years after it was first detected. The causative agents, legionellae, are freshwater bacteria with a fascinating ecology. These bacteria are intracellular pathogens of freshwater protozoa and utilize a similar mechanism to infect human phagocytic cells. There have been major advances in delineating the pathogenesis of legionellae through the identification of genes which allow the organism to bypass the endocytic pathways of both protozoan and human cells. Other bacteria that may share this novel infectious process are Coxiella burnetti and Brucella spp. More than 40 species and numerous serogroups of legionellae have been identified. Most diagnostic tests are directed at the species that causes most of the reported human cases of legionellosis, L. pneumophila serogroup 1. For this reason, information on the incidence of human respiratory disease attributable to other species and serogroups of legionellae is lacking. Improvements in diagnostic tests such as the urine antigen assay have inadvertently caused a decrease in the use of culture to detect infection, resulting in incomplete surveillance for legionellosis. Large, focal outbreaks of Legionnaires' disease continue to occur worldwide, and there is a critical need for surveillance for travel-related legionellosis in the United States. There is optimism that newly developed guidelines and water treatment practices can greatly reduce the incidence of this preventable illness.
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            Microorganisms resistant to free-living amoebae.

            Free-living amoebae feed on bacteria, fungi, and algae. However, some microorganisms have evolved to become resistant to these protists. These amoeba-resistant microorganisms include established pathogens, such as Cryptococcus neoformans, Legionella spp., Chlamydophila pneumoniae, Mycobacterium avium, Listeria monocytogenes, Pseudomonas aeruginosa, and Francisella tularensis, and emerging pathogens, such as Bosea spp., Simkania negevensis, Parachlamydia acanthamoebae, and Legionella-like amoebal pathogens. Some of these amoeba-resistant bacteria (ARB) are lytic for their amoebal host, while others are considered endosymbionts, since a stable host-parasite ratio is maintained. Free-living amoebae represent an important reservoir of ARB and may, while encysted, protect the internalized bacteria from chlorine and other biocides. Free-living amoebae may act as a Trojan horse, bringing hidden ARB within the human "Troy," and may produce vesicles filled with ARB, increasing their transmission potential. Free-living amoebae may also play a role in the selection of virulence traits and in adaptation to survival in macrophages. Thus, intra-amoebal growth was found to enhance virulence, and similar mechanisms seem to be implicated in the survival of ARB in response to both amoebae and macrophages. Moreover, free-living amoebae represent a useful tool for the culture of some intracellular bacteria and new bacterial species that might be potential emerging pathogens.
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              Systematic artifacts in metagenomes from complex microbial communities.

              Metagenomics is providing an unprecedented view of the taxonomic diversity, metabolic potential and ecological role of microbial communities in biomes as diverse as the mammalian gastrointestinal tract, the marine water column and soils. However, we have found a systematic error in metagenomes generated by 454-based pyrosequencing that leads to an overestimation of gene and taxon abundance; between 11% and 35% of sequences in a typical metagenome are artificial replicates. Here we document the error in several published and original datasets and offer a web-based solution (http://microbiomes.msu.edu/replicates) for identifying and removing these artifacts.
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                Author and article information

                Contributors
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                30 November 2017
                2017
                : 7
                : 477
                Affiliations
                [1] 1Department of Biological Chemistry, Johns Hopkins University School of Medicine , Baltimore, MD, United States
                [2] 2Department of Biochemistry, University of Toronto , Toronto, ON, Canada
                [3] 3Department of Molecular Genetics, University of Toronto , Toronto, ON, Canada
                [4] 4Public Health Ontario , Toronto, ON, Canada
                Author notes

                Edited by: Hayley J. Newton, University of Melbourne, Australia

                Reviewed by: Ascel Samba-Louaka, University of Poitiers, France; Ombeline Rossier, Université Paris-Sud, France

                *Correspondence: Tamara J. O'Connor toconno7@ 123456jhmi.edu
                Alexander W. Ensminger alex.ensminger@ 123456utoronto.ca
                Article
                10.3389/fcimb.2017.00477
                5714891
                29250488
                60d6be46-e28c-44fa-9d00-52dbafadb1d7
                Copyright © 2017 Boamah, Zhou, Ensminger and O'Connor.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 September 2017
                : 31 October 2017
                Page count
                Figures: 1, Tables: 2, Equations: 0, References: 140, Pages: 17, Words: 11770
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: 1R21AI119580
                Funded by: Natural Sciences and Engineering Research Council of Canada 10.13039/501100000038
                Award ID: RGPIN-2014-03641
                Categories
                Microbiology
                Review

                Infectious disease & Microbiology
                legionella,amoebae,protozoa,host range,environment,acanthamoebae,hartmannella,naegleria

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