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Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes

Legionella pneumophila, a causative agent of Legionnaires’ disease, is a facultative intracellular parasite of freshwater protozoa. Legionella pneumophila features a unique developmental network that involves several developmental forms including the infectious cyst forms. Reservoirs of L. pneumophi...

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Autores principales: Hellinga, Jacqueline R, Garduño, Rafael A, Kormish, Jay D, Tanner, Jennifer R, Khan, Deirdre, Buchko, Kristyn, Jimenez, Celine, Pinette, Mathieu M, Brassinga, Ann Karen C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4554460/
https://www.ncbi.nlm.nih.gov/pubmed/26131925
http://dx.doi.org/10.1002/mbo3.271
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author Hellinga, Jacqueline R
Garduño, Rafael A
Kormish, Jay D
Tanner, Jennifer R
Khan, Deirdre
Buchko, Kristyn
Jimenez, Celine
Pinette, Mathieu M
Brassinga, Ann Karen C
author_facet Hellinga, Jacqueline R
Garduño, Rafael A
Kormish, Jay D
Tanner, Jennifer R
Khan, Deirdre
Buchko, Kristyn
Jimenez, Celine
Pinette, Mathieu M
Brassinga, Ann Karen C
author_sort Hellinga, Jacqueline R
collection PubMed
description Legionella pneumophila, a causative agent of Legionnaires’ disease, is a facultative intracellular parasite of freshwater protozoa. Legionella pneumophila features a unique developmental network that involves several developmental forms including the infectious cyst forms. Reservoirs of L. pneumophila include natural and man-made freshwater systems; however, recent studies have shown that isolates of L. pneumophila can also be obtained directly from garden potting soil suggesting the presence of an additional reservoir. A previous study employing the metazoan Caenorhabditis elegans, a member of the Rhabditidae family of free-living soil nematodes, demonstrated that the intestinal lumen can be colonized with L. pneumophila. While both replicative forms and differentiated forms were observed in C. elegans, these morphologically distinct forms were initially observed to be restricted to the intestinal lumen. Using live DIC imaging coupled with focused transmission electron microscopy analyses, we report here that L. pneumophila is able to invade and establish Legionella-containing vacuoles (LCVs) in the intestinal cells. In addition, LCVs containing replicative and differentiated cyst forms were observed in the pseudocoelomic cavity and gonadal tissue of nematodes colonized with L. pneumophila. Furthermore, establishment of LCVs in the gonadal tissue was Dot/Icm dependent and required the presence of the endocytic factor RME-1 to gain access to maturing oocytes. Our findings are novel as this is the first report, to our knowledge, of extraintestinal LCVs containing L. pneumophila cyst forms in C. elegans tissues, highlighting the potential of soil-dwelling nematodes as an alternate environmental reservoir for L. pneumophila.
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spelling pubmed-45544602015-09-03 Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes Hellinga, Jacqueline R Garduño, Rafael A Kormish, Jay D Tanner, Jennifer R Khan, Deirdre Buchko, Kristyn Jimenez, Celine Pinette, Mathieu M Brassinga, Ann Karen C Microbiologyopen Original Research Legionella pneumophila, a causative agent of Legionnaires’ disease, is a facultative intracellular parasite of freshwater protozoa. Legionella pneumophila features a unique developmental network that involves several developmental forms including the infectious cyst forms. Reservoirs of L. pneumophila include natural and man-made freshwater systems; however, recent studies have shown that isolates of L. pneumophila can also be obtained directly from garden potting soil suggesting the presence of an additional reservoir. A previous study employing the metazoan Caenorhabditis elegans, a member of the Rhabditidae family of free-living soil nematodes, demonstrated that the intestinal lumen can be colonized with L. pneumophila. While both replicative forms and differentiated forms were observed in C. elegans, these morphologically distinct forms were initially observed to be restricted to the intestinal lumen. Using live DIC imaging coupled with focused transmission electron microscopy analyses, we report here that L. pneumophila is able to invade and establish Legionella-containing vacuoles (LCVs) in the intestinal cells. In addition, LCVs containing replicative and differentiated cyst forms were observed in the pseudocoelomic cavity and gonadal tissue of nematodes colonized with L. pneumophila. Furthermore, establishment of LCVs in the gonadal tissue was Dot/Icm dependent and required the presence of the endocytic factor RME-1 to gain access to maturing oocytes. Our findings are novel as this is the first report, to our knowledge, of extraintestinal LCVs containing L. pneumophila cyst forms in C. elegans tissues, highlighting the potential of soil-dwelling nematodes as an alternate environmental reservoir for L. pneumophila. John Wiley & Sons, Ltd 2015-08 2015-07-01 /pmc/articles/PMC4554460/ /pubmed/26131925 http://dx.doi.org/10.1002/mbo3.271 Text en © 2015 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd. http://creativecommons.org/licenses/by/4.0/ This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Hellinga, Jacqueline R
Garduño, Rafael A
Kormish, Jay D
Tanner, Jennifer R
Khan, Deirdre
Buchko, Kristyn
Jimenez, Celine
Pinette, Mathieu M
Brassinga, Ann Karen C
Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes
title Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes
title_full Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes
title_fullStr Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes
title_full_unstemmed Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes
title_short Identification of vacuoles containing extraintestinal differentiated forms of Legionella pneumophila in colonized Caenorhabditis elegans soil nematodes
title_sort identification of vacuoles containing extraintestinal differentiated forms of legionella pneumophila in colonized caenorhabditis elegans soil nematodes
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4554460/
https://www.ncbi.nlm.nih.gov/pubmed/26131925
http://dx.doi.org/10.1002/mbo3.271
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