Molecular survey and characterization of a novel Anaplasma species closely related to Anaplasma capra in ticks, northwestern China

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Abstract

Background

Anaplasma spp. are tick-transmitted bacteria that infect a wide variety of wild and domestic animals. These pathogens exhibit a high degree of biological diversity, broad geographical distribution, and represent a serious threat to veterinary and public health worldwide.

Results

A novel Anaplasma species was identified in Haemaphysalis qinghaiensis (Ixodidae) in northwestern China and was molecularly characterized by comparison of 16S rRNA, gltA, and groEL gene sequences. Of the 414 samples tested, 24 (5.8%) were positive for this Anaplasma species. On the basis of the 16S rRNA gene, this organism has been found to be closely related to and exhibit the highest sequence similarity with A. capra (99.8–99.9%) that was identified in goats and humans in northern China, but was distinct from other known Anaplasma species. Sequence analysis of the gltA and groEL genes revealed that this Anaplasma species was distinct from A. capra considering the lower sequence identity (88.6–88.7% for gltA and 90.6–91.0% for groEL) and a divergent phylogenetic position. Therefore, we described this Anaplasma species as A. capra-like bacteria.

Conclusions

The present study reports a potential novel Anaplasma species closely related to A. capra in H. qinghaiensis in northwestern China. The zoonotic potential of A. capra-like bacteria needs to be further determined.

Related collections

Most cited references 21

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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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Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease.

S Chen, J Dumler, J. S. Bakken … (1994)

Six patients from northern Minnesota and Wisconsin with a febrile illness accompanied by granulocytic cytoplasmic morulae suggestive of ehrlichial infection were identified. Two patients died, and splenic granulocytes of one patient contained cytoplasmic vacuoles with organisms ultrastructurally characteristic of ehrlichiae. From one patient, a 1.5-kb DNA product was amplified by PCR with universal eubacterial primers of 16S rDNA. Analysis of the nucleotide sequence of the amplified product revealed 99.9 and 99.8% similarities with E. phagocytophila and E. equi, respectively, neither of which has previously been known to infect humans. From the variable regions of the determined sequence, a forward primer specific for three organisms (human granulocytic ehrlichia, E. phagocytophila, and E. equi) and a reverse primer for these ehrlichiae and E. platys were designed. By nested PCR with amplification by the universal primers and then reamplification with the specific primers described above, the expected 919-bp product was generated from the blood of the index patient and three additional patients. Blood from these four patients and two more patients with granulocytic morulae contained DNA which was amplified by nested PCR involving a combination of a universal primer and the human granulocytic ehrlichia-E. phagocytophila-E. equi-E. platys group-specific primer. This apparently vector-borne human granulocytic ehrlichia has only 92.5% 16S rDNA homology with E. chaffeensis. Nested PCR with group-specific primers did not amplify E. chaffeensis DNA, and E. chaffeensis-specific primers did not amplify DNAs of the human granulocytic ehrlichia. Thus, six patients were shown to be infected by an Ehrlichia species never previously reported to infect humans.

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Emerging tick-borne infections in mainland China: an increasing public health threat

Li-Qun Fang, Kun Liu, Xin-Lou Li … (2015)

Summary Since the beginning of the 1980s, 33 emerging tick-borne agents have been identified in mainland China, including eight species of spotted fever group rickettsiae, seven species in the family Anaplasmataceae, six genospecies in the complex Borrelia burgdorferi sensu lato, 11 species of Babesia, and the virus causing severe fever with thrombocytopenia syndrome. In this Review we have mapped the geographical distributions of human cases of infection. 15 of the 33 emerging tick-borne agents have been reported to cause human disease, and their clinical characteristics have been described. The non-specific clinical manifestations caused by tick-borne pathogens present a major diagnostic challenge and most physicians are unfamiliar with the many tick-borne diseases that present with non-specific symptoms in the early stages of the illness. Advances in and application of modern molecular techniques should help with identification of emerging tick-borne pathogens and improve laboratory diagnosis of human infections. We expect that more novel tick-borne infections in ticks and animals will be identified and additional emerging tick-borne diseases in human beings will be discovered.

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Author and article information

Contributors

Jifei Yang: yangjifei@caas.cn

Zhijie Liu: liuzhijie@caas.cn

Qingli Niu: niuqingli@163.com

Junlong Liu: liujunlong@caas.cn

Rong Han: hanrong1715428@126.com

Guangyuan Liu: liuguangyuan@caas.cn

Yaoxu Shi: vvbdggyx@163.com

Jianxun Luo: luojianxun@caas.cn

Hong Yin: yinhong@caas.cn

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): 25 November 2016

Publication date PMC-release: 25 November 2016

Publication date Collection: 2016

Volume: 9

Electronic Location Identifier: 603

Affiliations

[1 ]State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Science, Xujiaping 1, Lanzhou, Gansu 730046 People’s Republic of China

[2 ]Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, 225009 People’s Republic of China

[3 ]China Agricultural Veterinary Biological Sciences and Technology Co., Ltd, Lanzhou, Gansu 730046 People’s Republic of China

Article

Publisher ID: 1886

DOI: 10.1186/s13071-016-1886-6

PMC ID: 5123347

PubMed ID: 27884197

SO-VID: b41e5444-5208-40f6-b380-062dac0d38ed

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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 : 29 August 2016

Date accepted : 11 November 2016

Funding

Funded by: NSFC

Award ID: 31502091

Award Recipient : Jifei Yang

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: anaplasma,16s rrna gene,glta gene,groel gene,haemaphysalis qinghaiensis,a. capra-like bacteria,china

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: anaplasma, 16s rrna gene, glta gene, groel gene, haemaphysalis qinghaiensis, a. capra-like bacteria, china

Molecular survey and characterization of a novel Anaplasma species closely related to Anaplasma capra in ticks, northwestern China

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Abstract

Background

Results

Conclusions

Related collections

Ticks and tick-borne pathogens

Most cited references 21

Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease.

Emerging tick-borne infections in mainland China: an increasing public health threat

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