A new multiple-locus variable-number tandem repeat analysis reveals different clusters for Anaplasma phagocytophilum circulating in domestic and wild ruminants

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Abstract

Background

Anaplasma phagocytophilum is a tick-borne intragranulocytic alpha-proteobacterium. It is the causative agent of tick-borne fever in ruminants, and of human granulocytic anaplasmosis in humans, two diseases which are becoming increasingly recognized in Europe and the USA. However, while several molecular typing tools have been developed over the last years, few of them are appropriate for in-depth exploration of the epidemiological cycle of this bacterium. Therefore we have developed a Multiple-Locus Variable number tandem repeat (VNTR) Analysis typing technique for A. phagocytophilum.

Methods

Five VNTRs were selected based on the HZ human-derived strain genome, and were tested on the Webster human-derived strain and on 123 DNA samples: 67 from cattle, 7 from sheep, 15 from roe deer, 4 from red deer, 1 from a reindeer, 2 from horses, 1 from a dog, and 26 from ticks.

Results

From these samples, we obtained 84 different profiles, with a diversity index of 0.96 (0.99 for vertebrate samples, i.e. without tick samples). Our technique confirmed that A. phagocytophilum from roe deer or domestic ruminants belong to two different clusters, while A. phagocytophilum from red deer and domestic ruminants locate within the same cluster, questioning the respective roles of roe vs red deer as reservoir hosts for domestic ruminant strains in Europe. As expected, greater diversity was obtained between rather than within cattle herds.

Conclusions

Our technique has great potential to provide detailed information on A. phagocytophilum isolates, improving both epidemiological and phylogenic investigations, thereby helping in the development of relevant prevention and control measures.

Electronic supplementary material

The online version of this article (doi:10.1186/1756-3305-7-439) contains supplementary material, which is available to authorized users.

Related collections

Most cited references 70

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Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and 'HGE agent' as subjective synonyms of Ehrlichia phagocytophila.

J Dumler, A F Barbet, C Bekker … (2001)

The genera Anaplasma, Ehrlichia, Cowdria, Neorickettsia and Wolbachia encompass a group of obligate intracellular bacteria that reside in vacuoles of eukaryotic cells and were previously placed in taxa based upon morphological, ecological, epidemiological and clinical characteristics. Recent genetic analyses of 16S rRNA genes, groESL and surface protein genes have indicated that the existing taxa designations are flawed. All 16S rRNA gene and groESL sequences deposited in GenBank prior to 2000 and selected sequences deposited thereafter were aligned and phylogenetic trees and bootstrap values were calculated using the neighbour-joining method and compared with trees generated with maximum-probability, maximum-likelihood, majority-rule consensus and parsimony methods. Supported by bootstrap probabilities of at least 54%, 16S rRNA gene comparisons consistently clustered to yield four distinct clades characterized roughly as Anaplasma (including the Ehrlichia phagocytophila group, Ehrlichia platys and Ehrlichia bovis) with a minimum of 96.1% similarity, Ehrlichia (including Cowdria ruminantium) with a minimum of 97.7% similarity, Wolbachia with a minimum of 95.6% similarity and Neorickettsia (including Ehrlichia sennetsu and Ehrlichia risticii) with a minimum of 94.9% similarity. Maximum similarity between clades ranged from 87.1 to 94.9%. Insufficient differences existed among E. phagocytophila, Ehrlichia equi and the human granulocytic ehrlichiosis (HGE) agent to support separate species designations, and this group was at least 98.2% similar to any Anaplasma species. These 16S rRNA gene analyses are strongly supported by similar groESL clades, as well as biological and antigenic characteristics. It is proposed that all members of the tribes Ehrlichieae and Wolbachieae be transferred to the family Anaplasmataceae and that the tribe structure of the family Rickettsiaceae be eliminated. The genus Anaplasma should be emended to include Anaplasma (Ehrlichia) phagocytophila comb. nov. (which also encompasses the former E. equi and the HGE agent), Anaplasma (Ehrlichia) bovis comb. nov. and Anaplasma (Ehrlichia) platys comb. nov., the genus Ehrlichia should be emended to include Ehrlichia (Cowdria) ruminantium comb. nov. and the genus Neorickettsia should be emended to include Neorickettsia (Ehrlichia) risticii comb. nov. and Neorickettsia (Ehrlichia) sennetsu comb. nov.

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Emphasizing the ecology in parasite community ecology.

Amy Pedersen, Andy Fenton (2007)

In natural systems, individuals are often co-infected by many species of parasites. However, the significance of interactions between species and the processes that shape within-host parasite communities remain unclear. Studies of parasite community ecology are often descriptive, focusing on patterns of parasite abundance across host populations rather than on the mechanisms that underlie interactions within a host. These within-host interactions are crucial for determining the fitness and transmissibility of co-infecting parasite species. Here, we highlight how techniques from community ecology can be used to restructure the approaches used to study parasite communities. We discuss insights offered by this mechanistic approach that will be crucial for predicting the impact on wildlife and human health of disease control measures, climate change or novel parasite species introductions.

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Population biology of multihost pathogens.

M. E. Woolhouse, L Taylor, D. Haydon (2001)

The majority of pathogens, including many of medical and veterinary importance, can infect more than one species of host. Population biology has yet to explain why perceived evolutionary advantages of pathogen specialization are, in practice, outweighed by those of generalization. Factors that predispose pathogens to generalism include high levels of genetic diversity and abundant opportunities for cross-species transmission, and the taxonomic distributions of generalists and specialists appear to reflect these factors. Generalism also has consequences for the evolution of virulence and for pathogen epidemiology, making both much less predictable. The evolutionary advantages and disadvantages of generalism are so finely balanced that even closely related pathogens can have very different host range sizes.

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Author and article information

Contributors

Thibaud Dugat: tdugat@vet-alfort.fr

Amélie Chastagner: amelie.chastagner@clermont.inra.fr

Anne-Claire Lagrée: anneclaire.lagree@vet-alfort.fr

Elisabeth Petit: epetit@vet-alfort.fr

Benoît Durand: benoit.durand@anses.fr

Simon Thierry: simon.thierry@anses.fr

Fabien Corbière: f.corbiere@envt.fr

Hélène Verheyden: Helene.Verheyden@toulouse.inra.fr

Luc Chabanne: luc.chabanne@vetagrosup.fr

Xavier Bailly: xavier.bailly@clermont.inra.fr

Agnès Leblond: agnes.leblond@vetagro-sup.fr

Gwenaël Vourc’h: gwenael.vourch@clermont.inra.fr

Henri-Jean Boulouis: hjboulouis@vet-alfort.fr

Renaud Maillard: r.maillard@envt.fr

Nadia Haddad: nhaddad@vet-alfort.fr

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 16 September 2014

Publication date PMC-release: 16 September 2014

Publication date Collection: 2014

Volume: 7

Issue: 1

Electronic Location Identifier: 439

Affiliations

[ ]Université Paris-Est, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR ENVA Anses UPEC USC INRA, Maisons-Alfort, France

[ ]Institut national de la recherche agronomique, UR 346 Épidémiologie Animale, Saint Genès Champanelle, France

[ ]Université Paris-Est, Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail, Laboratoire de Santé Animale, Unité d’Epidémiologie, Maisons-Alfort, France

[ ]Université Paris-Est, Agence nationale de sécurité sanitaire de l’alimentation de l’environnement et du travail, Laboratoire de Santé Animale, Unité des Zoonoses Bactériennes, Maisons-Alfort, France

[ ]Ecole Nationale Veterinaire de Toulouse, UMR 1225 Interactions Hotes Agents Pathogènes INRA-ENVT, Toulouse, France

[ ]Institut National de la Recherche Agronomique, UR 035 Comportement et Ecologie de la Faune Sauvage, Castanet-Tolosan, France

[ ]Université de Lyon VetAgroSup, Département des Animaux de compagnie, JE Hémopathogènes vectorisés, Marcy l’Etoile, France

[ ]Département Hippique, Université de Lyon VetAgroSup, Marcy l’Etoile, France

[ ]Ecole Nationale Veterinaire de Toulouse, Unité pathologie des ruminants, Toulouse, France

Article

Publisher ID: 1613

DOI: 10.1186/1756-3305-7-439

PMC ID: 4262125

PubMed ID: 25228371

SO-VID: ee823e46-f24c-4c81-9041-986565de88e6

License:

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 19 May 2014

Date accepted : 2 September 2014

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: anaplasma phagocytophilum,mlva,vntr,epidemiology,reservoir,wild ruminants,domestic ruminants

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: anaplasma phagocytophilum, mlva, vntr, epidemiology, reservoir, wild ruminants, domestic ruminants

A new multiple-locus variable-number tandem repeat analysis reveals different clusters for Anaplasma phagocytophilum circulating in domestic and wild ruminants

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Abstract

Background

Methods

Results

Conclusions

Electronic supplementary material

Related collections

Ticks and tick-borne pathogens

Most cited references 70

Emphasizing the ecology in parasite community ecology.

Population biology of multihost pathogens.

Author and article information

Contributors

Journal

Affiliations

Article

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Custom metadata

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