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A comparative ‘omics approach to candidate pathogenicity factor discovery in the brain-eating amoeba Naegleria fowleri

Emily K. Herman, Alex Greninger, Mark van der Giezen, Michael L. Ginger, Inmaculada Ramirez-Macias, Haylea C. Miller, Matthew J. Morgan, View ORCID ProfileAnastasios D. Tsaousis, Katrina Velle, Romana Vargová, Sebastian Rodrigo Najle, Georgina MacIntyre, Norbert Muller, Mattias Wittwer, Denise C. Zysset-Burri, Marek Elias, Claudio Slamovits, Matthew Weirauch, Lillian Fritz-Laylin, Francine Marciano-Cabral, Geoffrey J. Puzon, Tom Walsh, Charles Chiu, Joel B. Dacks
doi: https://doi.org/10.1101/2020.01.16.908186
Emily K. Herman
1Division of Infectious Disease, Department of Medicine, Faculty of Medicine and Dentistry, University of Alberta
2Department of Agricultural, Food and Nutritional Science, University of Alberta
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  • For correspondence: dacks@ualberta.ca
Alex Greninger
3Laboratory Medicine and Medicine / Infectious Diseases, UCSF-Abbott Viral Diagnostics and Discovery Center, UCSF Clinical Microbiology Laboratory UCSF School of Medicine
4Department of Laboratory Medicine, University of Washington Medical Center
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Mark van der Giezen
5Centre for Organelle Research, University of Stavanger
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Michael L. Ginger
6School of Applied Sciences, Department of Biological and Geographical Sciences, University of Huddersfield
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Inmaculada Ramirez-Macias
1Division of Infectious Disease, Department of Medicine, Faculty of Medicine and Dentistry, University of Alberta
7Department of Cardiology, Hospital Clinico Universitario Virgen de la Arrixaca. Instituto Murciano de Investigación Biosanitaria. Centro de Investigación Biomedica en Red-Enfermedades Cardiovasculares (CIBERCV)
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Haylea C. Miller
8CSIRO Land and Water
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Matthew J. Morgan
9CSIRO Land and Water, Black Mountain Laboratories
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Anastasios D. Tsaousis
10Laboratory of Molecular and Evolutionary Parasitology, RAPID group, School of Biosciences, University of Kent, Canterbury, UK
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  • ORCID record for Anastasios D. Tsaousis
Katrina Velle
11Department of Biology, University of Massachusetts
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Romana Vargová
12Department of Biology and Ecology, Faculty of Science, University of Ostrava
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Sebastian Rodrigo Najle
13Institut de Biologia Evolutiva (UPF-CSIC)
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Georgina MacIntyre
14Department of Medicine, Faculty of Medicine and Dentistry, University of Alberta
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Norbert Muller
15Institute of Parasitology, Vetsuisse Faculty Bern, University of Bern
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Mattias Wittwer
16Spiez Laboratory, Federal Office for Civil Protection, Austrasse, Spiez, Switzerland
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Denise C. Zysset-Burri
17Department of Ophthalmology, Inselspital, Bern University Hospital, University of Bern
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Marek Elias
12Department of Biology and Ecology, Faculty of Science, University of Ostrava
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Claudio Slamovits
18Department of Biochemistry and Molecular Biology, Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University
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Matthew Weirauch
19Center for Autoimmune Genomics and Etiology and Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA, Department of Pediatrics, University of Cincinnati College of Medicine
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Lillian Fritz-Laylin
11Department of Biology, University of Massachusetts
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Francine Marciano-Cabral
20Department of Microbiology and Immunology, Virginia Commonwealth University School of Medicine
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Geoffrey J. Puzon
8CSIRO Land and Water
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Tom Walsh
9CSIRO Land and Water, Black Mountain Laboratories
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Charles Chiu
3Laboratory Medicine and Medicine / Infectious Diseases, UCSF-Abbott Viral Diagnostics and Discovery Center, UCSF Clinical Microbiology Laboratory UCSF School of Medicine
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Joel B. Dacks
1Division of Infectious Disease, Department of Medicine, Faculty of Medicine and Dentistry, University of Alberta
21Department of Life Sciences, The Natural History Museum
22Institute of Parasitology, Biology Centre, Czech Academy of Sciences
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  • For correspondence: dacks@ualberta.ca
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Abstract

Of the 40 described Naegleria species, only N. fowleri can establish infection in humans, killing almost invariably within two weeks. In the brain, the amoeba performs piece-meal ingestion, or trogocytosis, of brain material causing massive inflammation. Conversely, its close relative Naegleria gruberi, which is used as a laboratory model organism, is non-pathogenic. The exact pathogenicity factors distinguishing N. fowleri from its harmless relatives are unclear. We have here taken an -omics approach to understanding N. fowleri biology and infection at the system level. We provide the first analysis of genomic diversity between strains, finding little conservation in synteny but high conservation in protein complement. We also demonstrate that the N. fowleri genome encodes a similarly complete cellular repertoire to that found in N. gruberi. Our comparative genomic analysis, together with a transcriptomic analysis of low versus high pathogenicity N. fowleri cultured in a mouse infection model, allowed us to construct a model of cellular systems involved in pathogenicity and furthermore provides ~500 novel candidate pathogenicity factors in this currently rare but highly fatal pathogen.

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A comparative ‘omics approach to candidate pathogenicity factor discovery in the brain-eating amoeba Naegleria fowleri
Emily K. Herman, Alex Greninger, Mark van der Giezen, Michael L. Ginger, Inmaculada Ramirez-Macias, Haylea C. Miller, Matthew J. Morgan, Anastasios D. Tsaousis, Katrina Velle, Romana Vargová, Sebastian Rodrigo Najle, Georgina MacIntyre, Norbert Muller, Mattias Wittwer, Denise C. Zysset-Burri, Marek Elias, Claudio Slamovits, Matthew Weirauch, Lillian Fritz-Laylin, Francine Marciano-Cabral, Geoffrey J. Puzon, Tom Walsh, Charles Chiu, Joel B. Dacks
bioRxiv 2020.01.16.908186; doi: https://doi.org/10.1101/2020.01.16.908186
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A comparative ‘omics approach to candidate pathogenicity factor discovery in the brain-eating amoeba Naegleria fowleri
Emily K. Herman, Alex Greninger, Mark van der Giezen, Michael L. Ginger, Inmaculada Ramirez-Macias, Haylea C. Miller, Matthew J. Morgan, Anastasios D. Tsaousis, Katrina Velle, Romana Vargová, Sebastian Rodrigo Najle, Georgina MacIntyre, Norbert Muller, Mattias Wittwer, Denise C. Zysset-Burri, Marek Elias, Claudio Slamovits, Matthew Weirauch, Lillian Fritz-Laylin, Francine Marciano-Cabral, Geoffrey J. Puzon, Tom Walsh, Charles Chiu, Joel B. Dacks
bioRxiv 2020.01.16.908186; doi: https://doi.org/10.1101/2020.01.16.908186

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