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Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles

BACKGROUND: The zoonotic intracellular alpha-proteobacterium Anaplasma phagocytophilum is a tick-transmitted pathogen. The associations between vertebrate reservoirs and vectors are described as wide-ranging, and it was previously shown that the pathogenicity of A. phagocytophilum differs depending...

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Autores principales: Fröhlich, Julia, Fischer, Susanne, Bauer, Benjamin, Hamel, Dietmar, Kohn, Barbara, Ahlers, Marion, Obiegala, Anna, Overzier, Evelyn, Pfeffer, Martin, Pfister, Kurt, Răileanu, Cristian, Rehbein, Steffen, Skuballa, Jasmin, Silaghi, Cornelia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433637/
https://www.ncbi.nlm.nih.gov/pubmed/37587504
http://dx.doi.org/10.1186/s13071-023-05900-3
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author Fröhlich, Julia
Fischer, Susanne
Bauer, Benjamin
Hamel, Dietmar
Kohn, Barbara
Ahlers, Marion
Obiegala, Anna
Overzier, Evelyn
Pfeffer, Martin
Pfister, Kurt
Răileanu, Cristian
Rehbein, Steffen
Skuballa, Jasmin
Silaghi, Cornelia
author_facet Fröhlich, Julia
Fischer, Susanne
Bauer, Benjamin
Hamel, Dietmar
Kohn, Barbara
Ahlers, Marion
Obiegala, Anna
Overzier, Evelyn
Pfeffer, Martin
Pfister, Kurt
Răileanu, Cristian
Rehbein, Steffen
Skuballa, Jasmin
Silaghi, Cornelia
author_sort Fröhlich, Julia
collection PubMed
description BACKGROUND: The zoonotic intracellular alpha-proteobacterium Anaplasma phagocytophilum is a tick-transmitted pathogen. The associations between vertebrate reservoirs and vectors are described as wide-ranging, and it was previously shown that the pathogenicity of A. phagocytophilum differs depending on the combination of pathogen variant and infected host species. This leads to the question of whether there are variations in particular gene loci associated with different virulence. Therefore, this study aims at clarifying existing host-variant combinations and detecting possible reservoir hosts. To understand these interactions, a complex toolset for molecular epidemiology, phylogeny and network theory was applied. METHODS: Sequences of up to four gene loci (msp4, msp2, groEL and 16S rRNA) were evaluated for different isolates from variable host species, including, for example, dogs, cattle and deer. Variant typing was conducted for each gene locus individually, and combinations of different gene loci were analysed to gain more detailed information about the genetic plasticity of A. phagocytophilum. Results were displayed as minimum spanning nets and correlation nets. RESULTS: The highest diversity of variants for all gene loci was observed in roe deer. In cattle, a reduced number of variants for 16S rRNA [only 16S-20(W) and 16S-22(Y)] but multiple variants of msp4 and groEL were found. For dogs, two msp4 variants [m4-20 and m4-2(B/C)] were found to be linked to different variants of the other three gene loci, creating two main combinations of gene loci variants. Cattle are placed centrally in the minimum spanning net analyses, indicating a crucial role in the transmission cycles by possibly bridging the vector-wildlife cycle to infections of humans and domestic animals. The minimum spanning nets confirmed previously described epidemiological cycles of the bacterium in Europe, showing separation of variants originating from wildlife animals only and a set of variants shared by wild and domestic animals. CONCLUSIONS: In this comprehensive study of 1280 sequences, we found a high number of gene variants only occurring in specific hosts. Additionally, different hosts show unique but also shared variant combinations. The use of our four gene loci expand the knowledge of host–pathogen interactions and may be a starting point to predict future spread and infection risks of A. phagocytophilum in Europe. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05900-3.
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spelling pubmed-104336372023-08-18 Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles Fröhlich, Julia Fischer, Susanne Bauer, Benjamin Hamel, Dietmar Kohn, Barbara Ahlers, Marion Obiegala, Anna Overzier, Evelyn Pfeffer, Martin Pfister, Kurt Răileanu, Cristian Rehbein, Steffen Skuballa, Jasmin Silaghi, Cornelia Parasit Vectors Research BACKGROUND: The zoonotic intracellular alpha-proteobacterium Anaplasma phagocytophilum is a tick-transmitted pathogen. The associations between vertebrate reservoirs and vectors are described as wide-ranging, and it was previously shown that the pathogenicity of A. phagocytophilum differs depending on the combination of pathogen variant and infected host species. This leads to the question of whether there are variations in particular gene loci associated with different virulence. Therefore, this study aims at clarifying existing host-variant combinations and detecting possible reservoir hosts. To understand these interactions, a complex toolset for molecular epidemiology, phylogeny and network theory was applied. METHODS: Sequences of up to four gene loci (msp4, msp2, groEL and 16S rRNA) were evaluated for different isolates from variable host species, including, for example, dogs, cattle and deer. Variant typing was conducted for each gene locus individually, and combinations of different gene loci were analysed to gain more detailed information about the genetic plasticity of A. phagocytophilum. Results were displayed as minimum spanning nets and correlation nets. RESULTS: The highest diversity of variants for all gene loci was observed in roe deer. In cattle, a reduced number of variants for 16S rRNA [only 16S-20(W) and 16S-22(Y)] but multiple variants of msp4 and groEL were found. For dogs, two msp4 variants [m4-20 and m4-2(B/C)] were found to be linked to different variants of the other three gene loci, creating two main combinations of gene loci variants. Cattle are placed centrally in the minimum spanning net analyses, indicating a crucial role in the transmission cycles by possibly bridging the vector-wildlife cycle to infections of humans and domestic animals. The minimum spanning nets confirmed previously described epidemiological cycles of the bacterium in Europe, showing separation of variants originating from wildlife animals only and a set of variants shared by wild and domestic animals. CONCLUSIONS: In this comprehensive study of 1280 sequences, we found a high number of gene variants only occurring in specific hosts. Additionally, different hosts show unique but also shared variant combinations. The use of our four gene loci expand the knowledge of host–pathogen interactions and may be a starting point to predict future spread and infection risks of A. phagocytophilum in Europe. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-023-05900-3. BioMed Central 2023-08-16 /pmc/articles/PMC10433637/ /pubmed/37587504 http://dx.doi.org/10.1186/s13071-023-05900-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Fröhlich, Julia
Fischer, Susanne
Bauer, Benjamin
Hamel, Dietmar
Kohn, Barbara
Ahlers, Marion
Obiegala, Anna
Overzier, Evelyn
Pfeffer, Martin
Pfister, Kurt
Răileanu, Cristian
Rehbein, Steffen
Skuballa, Jasmin
Silaghi, Cornelia
Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles
title Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles
title_full Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles
title_fullStr Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles
title_full_unstemmed Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles
title_short Host–pathogen associations revealed by genotyping of European strains of Anaplasma phagocytophilum to describe natural endemic cycles
title_sort host–pathogen associations revealed by genotyping of european strains of anaplasma phagocytophilum to describe natural endemic cycles
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433637/
https://www.ncbi.nlm.nih.gov/pubmed/37587504
http://dx.doi.org/10.1186/s13071-023-05900-3
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