Open Access

Insight into the genetic diversity of Anaplasma marginale in cattle from ten provinces of China

  • Jifei Yang1,
  • Rong Han1,
  • Zhijie Liu1,
  • Qingli Niu1,
  • Guiquan Guan1,
  • Guangyuan Liu1,
  • Jianxun Luo1 and
  • Hong Yin1, 2Email author
Contributed equally
Parasites & Vectors201710:565

https://doi.org/10.1186/s13071-017-2485-x

Received: 4 July 2017

Accepted: 18 October 2017

Published: 13 November 2017

Abstract

Background

Anaplasma marginale is an important tick-transmitted rickettsial pathogen of cattle, with worldwide distribution and an important economic impact. The genetic diversity of A. marginale strains has been extensively characterized in different geographical regions throughout the world, while information is limited on studies in China. This study was carried out to determine the prevalence and genetic diversity of A. marginale strains in cattle from ten provinces of China.

Methods

A total of 557 blood samples from cattle were collected and screened for the occurrence of A. marginale by PCR based on the msp4 gene. The partial msp1a gene containing tandem repeat sequences was further amplified from msp4 positive samples. The Msp1a amino acid repeats were identified, and genetic variation of A. marginale strains was characterized based on the variation in the repeated portion of Msp1a.

Results

Our results showed that 31.6% of 557 cattle were positive for A. marginale. The infection rates of A. marginale varied considerably from 0 to 96.9% in different sampling regions. Sequence analysis revealed that two msp4 sequence variants of A. marginale exist in cattle. One hundred and three msp1a sequences were obtained and permitted to identify 42 Msp1a tandem repeats, 21 of which were not previously published for A. marginale. Moreover, 61 A. marginale genotypes were identified based on the structure of Msp1a tandem repeats.

Conclusions

Anaplasma marginale is widely distributed in China and a high prevalence of infection was observed in cattle. The geographical strains of A. marginale were molecularly characterized based on the structure of Msp1a tandem repeats. Forty-two Msp1a tandem repeats and 61 genotypes of A. marginale were identified. This study, for the first time, revealed the genetic diversity of A. marginale strains in cattle in China.

Keywords

Anaplasma marginale msp4 geneMsp1a tandem repeatsGenotypesCattleChina

Background

Anaplasma marginale is an obligate intraerythrocytic pathogen that cause bovine anaplasmosis throughout the world [1]. It was first described in cattle by Sir Arnold Theiler in 1910, and is widely distributed in Africa, Asia, Australia, South and Central America, southern Europe, and the USA [25]. Animals infected by A. marginale develop a mild to severe life-threatening hemolytic disease, causing considerable economic loss to the cattle industry worldwide [5]. The organism can be transmitted biologically by ticks and mechanically by blood-sucking arthropods or blood-contaminated fomites [6]. Approximately 20 tick species, mainly of the genera Rhipicephalus and Dermacentor, have been recorded as vectors of A. marginale [7]. Anaplasma marginale is host-specific, and cattle and water buffaloes are highly susceptible to infection [6, 8, 9]. The animals that recover from acute anaplasmosis develop persistent infection and act as reservoirs for this causative agent [1].

To date, a great number of geographical strains of A. marginale have been identified on a global scale, which vary in genotype, virulence, antigenic characteristics and infectivity for ticks [6]. Characterization of the genetic diversity of A. marginale strains has been performed based on the variability of tandem repeat amino acid sequences located in the N-terminal region of the major surface protein (Msp) 1a, and numerous geographical Msp1a tandem repeats and genotypes were identified [10]. In China, A. marginale has been recognized for over 30 years, and Rhipicephalus microplus is considered to be the most important tick vector with a nationwide distribution [11, 12]. Despite the importance of bovine anaplasmosis, limited information is available for A. marginale in China. Previously, the occurrence of A. marginale was reported in several provinces, and only one Msp1a tandem repeat (GenBank: DQ811774) was identified in A. marginale strain HB-A8 from cattle [1115]. The objective of this study was to determine the prevalence and genetic diversity of A. marginale strains in cattle from different geographical areas of China.

Methods

Study areas, sample collection and DNA isolation

This study was conducted between 2011 and 2015 in rural areas of 22 counties from ten provinces of China, including Inner Mongolia and Liaoning (north-east China); Hunan, Guangdong, Guangxi and Hainan (south-central China); Chongqing, Sichuan, Guizhou and Yunnan (south-west China). The sample sites are listed in Table 1. Animals for this study were randomly selected in two to three herds for each county. A total of 557 jugular blood samples were collected in vacutainer EDTA tubes from adult cattle. Genomic DNA was prepared from 300 μl blood samples using the Gentra Puregene Blood Kit (Qiagen, Beijing, China) following the protocols recommended by the producer. DNA was resuspended in the elution buffer provided in the commercial kit and stored at -20 °C until use.
Table 1

Detection of A. marginale in cattle from China, 2011–2015

 

Location

No. tested

No. positive (%)

Area

Province

County

South Central

Hunan

Yongzhou

18

2 (11.1)

Linli

36

0 (0)

Lianyuan

31

14 (45.2)

Guangdong

Qingyuan

25

23 (92.0)

Zhaoqing

24

19 (79.1)

Maoming

50

1 (2.0)

Guangxi

Baise

32

14 (43.8)

Tianyang

26

22 (84.6)

Chongzuo

12

7 (58.3)

Hainan

Chengmai

46

0 (0)

Subtotal

 

300

102 (34.0)

Southwest

Chongqing

Jiangjin

30

1 (3.3)

Wanzhou

25

3 (12.0)

Sichuan

Panzhihua

32

31 (96.9)

Guizhou

Dushan

30

18 (60.0)

Rongjiang

12

10 (83.3)

Yunnan

Yanshan

29

1 (3.4)

Ruili

17

0 (0)

Fuyuan

8

3 (37.5)

Subtotal

 

183

67 (36.6)

Northeast

Liaoning

Benxi

16

2 (12.5)

Anshan

29

0 (0)

Inner Mongolia

Xinbaerhuzuoqi

15

5 (33.3)

Eerguna

14

0 (0)

Subtotal

 

74

7 (9.5)

Total

 

557

176 (31.6)

PCR reactions

The extracted DNA was used for the amplification of msp4 gene of A. marginale by nested PCR [16, 17]. Briefly, the primers MSP43 (5′-GGG AGC TCC TAT GAA TTA CAG AGA ATT GTT TAC-3′) and MSP45 (5′-CCG GAT CCT TAG CTG AAC AGA ATC TTG C-3′) were used for the first round of PCR amplification, while AmargMSP4Fw (5′-CTG AAG GGG GAG TAA TGG G-3′) and AmargMSP4Rev (5′-GGT AAT AGC TGC CAG AGA TTC C-3′) were used in a nested-PCR reaction, which generated a fragment of 344 bp. The DNA extracted from cattle infected with A. marginale (isolate Lushi, GenBank: AJ633048) and sterile water was used as the positive and negative control, respectively. The partial msp1a gene containing the tandem repeats of A. marginale was further amplified from msp4-positive samples by PCR as reported previously [18] with some modifications. The outer primers 1733F (5′-TGT GCT TAT GGC AGA CAT TTC C-3′) and 3134R (5′-TCA CGG TCA AAA CCT TTG CTT ACC-3′) were used in the first reaction as described by Lew et al. [18]. An inner forward primer AM-F2 was designed in highly conserved region of msp1a sequences available in GenBank using OligoAnalyzer 3.1 (Integrated DNA Technologies, 2012, Iowa, USA). The inner primers AM-F2 (5′-CGT CTC ACA AGT TTG TAC GCT GTG C-3′, in this study) and 2957R (5′-AAA CCT TGT AGC CCC AAC TTA TCC-3′) were used in the second reaction [18]. The reactions were performed in an automatic thermocycler (Bio-Rad, Hercules, USA) with a final volume of 25 μl containing 2.0 μl template DNA. Thermal cycling comprised 4 min of an initial denaturation at 94 °C, 35 cycles of 94 °C for 30 s, annealing for 30 s (55 °C for 1733F/3134R, 60 °C for MSP43/MSP45, AmargMSP4Fw/AmargMSP4Rev and AM-F2/2957R) and 72 °C for 30–90 s (depending on the target fragments), and a final extension at 72 °C for 10 min. Amplified products were analyzed by 1.0% agarose gel electrophoresis.

Sequences and statistical analysis

The purified PCR amplicons of msp4 and msp1a genes of A. marginale were cloned into pGEM-T Easy vector (Promega, Madison, WI, USA). Two recombinants were selected randomly and sequenced (Genscript, Nanjing, China). Sequence analysis was performed using the BLASTn search and the ClustalW software (DNAStar, Madison, WI, USA). The A. marginale msp1a sequences were trimmed and translated to amino acids using CLC Genomics Workbench 7.5.1 (Qiagen, Aarhus, Denmark). The tandem repeats of A. marginale Msp1a amino acid sequences were identified and aligned by using the ClustalW software. Statistical analysis was conducted using a Chi-square test in PASW statistics 18.0 (SPSS, Chicago, IL, USA). P-values of 0.05 or less were considered statistically significant.

Nucleotide sequence accession numbers

The sequences obtained in this study were submitted to the GenBank database and provided accession numbers as follows: MF326686 and MF326687 for msp4 and MF326688–MF326790 for msp1a.

Results

Anaplasma marginale DNA was detected in 176 of 557 cattle, with an overall infection rate of 31.6% (Table 1). The infection rates of A. marginale varied considerably from 0 to 96.9% in different sampling regions. The infection was detected in 17 of 22 counties, representing all ten provinces included in this study. The infection rate of A. marginale in the south-west (67/183, 36.6%) was almost comparable with that in the south-central region (102/300, 34.0%) (χ 2 = 0.163, df = 1, P > 0.05), but was significantly higher than in the north-east (7/74, 9.5%) (χ 2 = 11.621, df = 1, P < 0.001).

Sequence analysis of msp4 gene confirmed the infections of A. marginale in cattle, and two msp4 sequence variants with 99.7% similarity were obtained in this study. The msp4 sequence variant 20-14c (GenBank MF326686) was identical to the A. marginale strains Tamaulipas, Kanchanaburi66 and 11-MSP43 (GenBank: EU283844, KU764497 and KX840009) from Mexico, Thailand and China, respectively [19]. The sequence variant 1-15a (GenBank: MF326687) has 99.7–100% identity to strains Nakhonpathom195 and AMSP4-HYD21 (GenBank: KU764498 and KX989532) from Thailand and India, respectively [20].

On the basis of the msp4 PCR results, A. marginale-positive samples were subjected for further analysis. One hundred and three msp1a sequences (GenBank: MF326688–MF326790) were obtained. Sequence analyses revealed that 97.1% (100/103) of A. marginale isolates contained the Msp1a tandem repeats, and 42 different types of Msp1a tandem repeats with 28 to 29 amino acids among Chinese A. marginale strains were identified (Fig. 1). Aside from Msp1a tandem repeats (M, F, τ, Ph9, Is1; 73, 13, 27, MGl10, 154, 103; Me1, 14, 72; 80, C, 3, 17, 10, LJ1, 22–2, 37, 4 and Ph2) with known name reported in previous studies [21], 21 new tandem repeats (designated as Ch1–21; Fig. 1) are described for the first time in this study.
Fig. 1

Alignment of Msp1a amino acid repeat sequences of A. marginale detected from Chinese cattle. The 42 repeat types were aligned using the ClustalW method in the MegAlign software. The Msp1a tandem repeats (M, F, τ, Ph9, Is1; 73, 13, 27, MGl10, 154, 103; Me1, 14, 72; 80, C, 3, 17, 10, LJ1, 22–2, 37, 4 and Ph2) identified herein have been reported in previous studies, and 21 new Msp1a tandem repeats were named as Ch1–21. The one letter code was used to reveal the different amino acid sequences of Msp1a repeats. The variable amino acids are highlighted on a black background and gaps indicate deletions/insertions

The genetic diversity of A. marginale strains was analyzed based on the Msp1a tandem repeats structure. A total of 103 A. marginale isolates were classified into 61 genotypes with a maximum repeat number of five (Table 2). Interestingly, three isolates (AM5-2a, AM5-2b and AM17-2b; GenBank: MF326718, MF326719 and MF326770) had no amino acid repeats (Table 2). The remaining 100 isolates contained one to five Msp1a tandem repeats. As shown in Table 2, five Msp1a tandem repeats were identified in five A. marginale isolates; four repeats in 23 isolates; three repeats in 26 isolates; two repeats in 32 isolates and a single repeat in 14 isolates (Table 2). Most of these Msp1a tandem repeats (Ch1, F, M, Ph9, etc.) were shared between different A. marginale isolates and genotypes, while some of them (Ch4, Ch5, Ch7, etc.) were unique and had a low frequency among these isolates (Table 2). In addition, 21 animals positive for A. marginale identified in this study were infected by more than one genotype.
Table 2

Organization of Msp1a tandem repeats in A. marginale strains identified in cattle

Strains

GenBank ID

Structure of Msp1a tandem repeats

AM1-10a

MF326688

Ch1

M

   

AM1-10b

MF326689

Ch1

F

M

M

 

AM1-102a

MF326690

Ch1

    

AM1-102b

MF326691

Ch1

    

AM3-10b

MF326692

τ

M

Ch2

  

AM3-21b

MF326693

Ph27

Is1; 73

Is1; 73

Is1; 73

Is1; 73

AM3-21c

MF326694

Ph27

Is1; 73

Is1; 73

Is1; 73

Is1; 73

AM3-27a

MF326695

13

27

27

27

 

AM3-27c

MF326696

13

27

27

  

AM4-1a

MF326697

Ch1

    

AM4-1b

MF326698

Ch1

    

AM4-2b

MF326699

Ch3

Ch2

Ch2

  

AM4-4a

MF326700

Ch1

    

AM4-4c

MF326701

Ch1

M

F

M

 

AM4-6a

MF326702

MGl10

154

   

AM4-7a

MF326703

2Is1; 73

Is1; 73

   

AM4-8a

MF326704

2Is1; 73

Is1; 73

   

AM4-9b

MF326705

2Is1; 73

Is1; 73

   

AM4-10b

MF326706

2Is1; 73

Is1; 73

   

AM4-12a

MF326707

Ch4

Ch5

   

AM4-12b

MF326708

Ch4

Ch5

   

AM4-15a

MF326709

Ch6

Ch2

Ch2

Ch2

 

AM4-15b

MF326710

M

M

103; Me1

  

AM4-17b

MF326711

Ph9

Is1; 73

   

AM4-18a

MF326712

Ch7

14

   

AM4-18b

MF326713

Ch7

14

   

AM4-21b

MF326714

72; 80

Ch8

Ch8

Ch8

Ch8

AM4-22b

MF326715

Ch7

14

   

AM4-23b

MF326716

27

Is1; 73

Is1; 73

  

AM4-24a

MF326717

Ch9

Ch3

Ch3

Ch3

 

AM5-2a

MF326718

     

AM5-2b

MF326719

     

AM5-4a

MF326720

Ch3

Ch2

Ch2

  

AM5-4b

MF326721

Ch1

M

   

AM5-6a

MF326722

13

    

AM5-6b

MF326723

Ch3

Ch2

Ch2

Ch2

 

AM5-8a

MF326724

F

M

M

  

AM5-8b

MF326725

Ch1

    

AM5-9b

MF326726

Ch1

M

F

M

 

AM5-11b

MF326727

Ph9

Is1; 73

Ch2

  

AM5-11c

MF326728

Ph9

Is1; 73

Is1; 73

Is1; 73

 

AM5-13c

MF326729

27

Is1; 73

   

AM5-15a

MF326730

27

Is1; 73

Is1; 73

  

AM5-15c

MF326731

27

Is1; 73

   

AM5-16b

MF326732

F

M

C

  

AM5-19a

MF326733

Ch1

M

F

M

 

AM5-19b

MF326734

Ch1

M

F

M

 

AM5-22a

MF326735

13

14

M

  

AM5-22c

MF326736

Ch1

M

F

M

 

AM6-7a

MF326737

Ch10

Is1; 73

Is1; 73

  

AM6-7b

MF326738

Ch10

Is1; 73

Is1; 73

  

AM7-8b

MF326739

F

M

M

  

AM8-5c

MF326740

27

Is1; 73

24

Is1; 73

 

AM9-3b

MF326741

3

    

AM9-3c

MF326742

103; Me1

3

3

  

AM9-5a

MF326743

13

17

Ch2

  

AM9-14a

MF326744

F

10

   

AM9-14b

MF326745

F

10

MG110

  

AM9-21a

MF326746

LJ1

22–2

27

14

 

AM9-24a

MF326747

M

F

   

AM9-24b

MF326748

Ph9

Is1; 73

Is1; 73

Is1; 73

Is1; 73

AM9-26b

MF326749

13

    

AM9-26c

MF326750

37

154

27

  

AM15-3b

MF326751

Ph9

Is1; 73

   

AM15-5a

MF326752

27

Is1; 73

Is1; 73

Is1; 73

 

AM15-5b

MF326753

27

Is1; 73

Is1; 73

Is1; 73

 

AM15-18a

MF326754

Ch12

Is1; 73

   

AM15-18b

MF326755

Ch12

Ch13

Ch13

Is1; 73

 

AM15-24a

MF326756

3

Ch2

   

AM15-30a

MF326757

M

M

M

M

 

AM15-30b

MF326758

13

4

   

AM16-1b

MF326759

Ch14

Ch2

   

AM16-2b

MF326760

13

14

   

AM16-2c

MF326761

13

14

   

AM16-5c

MF326762

Ph9

    

AM16-9b

MF326763

Ch15

Is1; 73

   

AM16-12b

MF326764

Ch10

Is1; 73

Is1; 73

  

AM16-14a

MF326765

13

14

   

AM16-14b

MF326766

13

14

   

AM16-21b

MF326767

13

14

   

AM16-25a

MF326768

Ch16

Ch17

Ch17

Is1; 73

Ch2

AM16-25b

MF326769

Ch18

Ch19

Is1; 73

Ch2

 

AM17-2b

MF326770

     

AM18-3b

MF326771

3

Is1; 73

Is1; 73

  

AM18-3c

MF326772

27

Is1; 73

Is1; 73

  

AM18-6b

MF326773

Ch20

13

   

AM18-8b

MF326774

M

Ch11

Ph9

  

AM18-15a

MF326775

13

    

AM18-15b

MF326776

4

4

3

  

AM18–19a

MF326777

Ch21

Is1; 73

Is1; 73

  

AM18–19

MF326778

F

F

   

AM18-20b

MF326779

Ch15

    

AM18-24b

MF326780

F

M

M

M

 

AM19-1b

MF326781

Ph9

Is1; 73

Is1; 73

  

AM19-1c

MF326782

Ph9

Is1; 73

   

AM19-2b

MF326783

Ph9

    

AM19-2c

MF326784

Ph9

    

AM19-4b

MF326785

Ph2

Is1; 73

Is1; 73

Is1; 73

 

AM19-6a

MF326786

Ph9

Is1; 73

Is1; 73

Is1; 73

 

AM19-6b

MF326787

Ph9

Is1; 73

Is1; 73

  

AM19-8b

MF326788

Ph9

Is1; 73

   

AM19-9c

MF326789

Ph9

Is1; 73

Is1; 73

Is1; 73

 

AM19-10a

MF326790

Ph9

Is1; 73

Is1; 73

Is1; 73

 

Discussion

Bovine anaplasmosis caused by A. marginale is widely distributed in tropical and subtropical areas throughout the world [22]. In China, A. marginale was first isolated from cattle as early as 1987 in Lushi County, Henan Province [11]. Since then, A. marginale has been detected in Hyalomma asiaticum ticks and cows from five farms in northwestern China [13]. A molecular survey of Anaplasma spp. has previously been conducted in domestic ruminants from 12 provinces of China, and A. marginale infection in cattle was identified by gltA sequencing [14]. In addition, this agent has also been found in cattle from Chongqing, southwestern China [15]. Those reports provided molecular evidence of A. marginale by genus-specific PCR and sequencing in domestic ruminants in China. However, information of epidemiology and molecular characterization of Chinese strains is limited. In the present study, a molecular survey of A. marginale was conducted by species-specific PCR in cattle, and 31.6% of 557 sampled animals were naturally infected with this organism. Since animals infected by A. marginale can develop a persistent infection that may facilitate the maintenance and further spread of infection [23], a high prevalence of A. marginale was relatively common in the vertebrate hosts. In this study, a significant difference in infection rates of A. marginale was observed between the South and the North area of China, and this may be mainly associated with the tick vectors. The geographical distribution of different tick species in China vary from South to North due to the diverse ecological environments, climate variability and hosts [24], affecting consequently the presence of tick-borne diseases. Anaplasma marginale was identified in all ten sampled provinces, indicating that this agent was widely distributed and may pose a serious threat to the cattle industry in China, which should arise extensive attention.

The members in the genus Anaplasma have diverse surface-exposed proteins [6]. There are six major surface proteins (MSPs) that have been well characterized in A. marginale, and were considered to be involved in the interactions of pathogen with both ticks and hosts [22, 25]. These major surface protein genes may evolve more obviously because of the selective pressure exerted by the host immune system [26]. The genetic variability of A. marginale was frequently characterized on the basis of the msp4 and msp1a genes [27]. However, the msp4 gene is highly conserved and stable among widely divergent strains of A. marginale [28]. In this study, the msp4 sequences of A. marginale isolates identified in cattle from different geographical regions shared high sequence identity (99.7 to 100%), and have previously been reported in cattle from other countries [19, 20].

Anaplasma marginale geographical strains differing in their biological properties have been genetically characterized, 234 Msp1a tandem repeats were identified and summarized recently by Catanese et al. [21], providing over 350 genotypes based on the structure of Msp1a amino acid repeats [21]. In the present study, a comparison of 103 isolates from different geographical regions permitted identification of 42 Msp1a tandem repeats, 50% of which were identical to those previously published for A. marginale strains. The Msp1a tandem repeats were not always clustered together corresponding to the geographical locations; some repeats have been identified in the A. marginale isolates from various regions and appeared to be distributed nationwide (Table 2). These findings suggest that there is no significant association between specific Msp1a repeats and geographical regions, and this may be attributed to movement of vectors and vertebrate hosts.

Anaplasma marginale geographical strains differ in the copy number and amino acid repeat sequences in Msp1a [29]. In our study, 61 A. marginale genotypes were identified based on the variation in the repeated portion of Msp1a, showcasing the broad genetic diversity of A. marginale in cattle in China. Previous reports have demonstrated that the Msp1a repeats contain functional domains that are involved in adhesion to tick cells and bovine erythrocytes [30]. They also contain B cell and neutralization epitopes that are critical for immune protection in animals [30], suggesting that Msp1a repeats play an important role in the invasion, transmission and survival of A. marginale. Generally, A. marginale strains contain at least one Msp1a tandem repeat (maximum number of 10) [6]; however, the repeat sequence was not found in three isolates from Guangdong and Guangxi Province in south-central China.

It has been demonstrated that the animals and ticks naturally infected with one genotype of A. marginale preclude infection with additional genotypes, indicating that different genotypes could not coexist in the same animals and ecosystems [31, 32]. This infection exclusion mechanism has also been revealed for Rickettsia species [33]. However, A. marginale strain superinfection with different Msp1a genotypes has been reported subsequently and proven to be associated with high levels of infection prevalence [3436]. In the present study, 21 animals positive for A. marginale were infected by multiple genotypes. This finding was consistent with the previous report [37], in which described distinct A. marginale strains circulated in the same animals and herd. A similar phenomenon was also observed for A. marginale subsp. centrale [38]. The coexistence of divergent A. marginale strains may serve as a potential source of variation.

In summary, our results revealed the prevalence and genetic diversity of A. marginale strains using Msp1a tandem repeats in ten provinces. As one of the most important tick-borne diseases, bovine anaplasmosis caused by A. marginale should no longer be neglected in endemic areas of China.

Conclusions

In the present study, 31.6% of 557 cattle from 22 counties of ten provinces were positive for A. marginale. The A. marginale strains were molecularly characterized based on the structure of Msp1a amino acid repeats. A total of 103 isolates were classified to 61 genotypes, and 42 Msp1a tandem repeats were identified, 21 of which have not previously been described. The present study, for the first time, revealed the genetic diversity of A. marginale strains using Msp1a repeat sequences in cattle in China.

Abbreviations

EDTA: 

ethylene diamine tetraacetic acid

Msp: 

major surface protein

UV: 

ultraviolet

Declarations

Acknowledgements

Not applicable.

Funding

This study was financially supported by the National Key Research and Development Program of China (2017YFD0501200, 2016YFC1202000, 2016YFC1202002); the NSFC (31502091); ASTIP, FRIP (2014ZL010), CAAS; 973 Program (2015CB150300); the Jiangsu Co-innovation Center program for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, and the State Key Laboratory of Veterinary Etiological Biology Project.

Availability of data and materials

The sequences obtained in this study were submitted to the GenBank database and provided accession numbers as follows: MF326686 and MF326687 for msp4 and MF326688–MF326790 for msp1a.

Authors’ contributions

HY and JY designed and coordinated this study. JY and RH drafted and revised the manuscript. JY, ZL, QN and GG collected the samples included in this study. RH, JY, QN, GL and JL conducted the experiments and data analysis. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Collection of cattle samples was approved by the owner, and animals were handled in accordance with the Animal Ethics Procedures and Guidelines. The study was approved by the Animal Ethics Committee of Lanzhou Veterinary Research Institute (Approval No. LVRIAEC2011–018).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Authors’ 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 Sciences
(2)
Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses

References

  1. Kocan KM, de la Fuente J, Guglielmone AA, Melendez RD. Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microbiol Rev. 2003;16(4):698–712.View ArticlePubMedPubMed CentralGoogle Scholar
  2. Theiler A. Gall-sickness of South Africa. (Anaplasmosis of cattle). J Comp Pathol. 1910;23:98–115.View ArticleGoogle Scholar
  3. Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129:S3–S14.View ArticlePubMedGoogle Scholar
  4. Atif FA. Anaplasma marginale and Anaplasma phagocytophilum: Rickettsiales pathogens of veterinary and public health significance. Parasitol Res. 2015;114(11):3941–57.View ArticlePubMedGoogle Scholar
  5. Aubry P, Geale DWA. Review of bovine anaplasmosis. Transbound Emerg Dis. 2011;58(1):1–30.View ArticlePubMedGoogle Scholar
  6. Battilani M, De Arcangeli S, Balboni A, Dondi F. Genetic diversity and molecular epidemiology of Anaplasma. Infect Genet Evol. 2017;49:195–211.View ArticlePubMedGoogle Scholar
  7. Rar V, Golovljova I. Anaplasma, Ehrlichia, and "Candidatus Neoehrlichia" bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect Genet Evol. 2011;11(8):1842–61.Google Scholar
  8. Silva JB, Cabezas-Cruz A, Fonseca AH, Barbosa JD, de la Fuente J. Infection of water buffalo in Rio de Janeiro Brazil with Anaplasma marginale strains also reported in cattle. Vet Parasitol. 2014;205(3–4):730–4.View ArticlePubMedGoogle Scholar
  9. Silva JB, Fonseca AH, Barbosa JD, Cabezas-Cruz A, de la Fuente J. Low genetic diversity associated with low prevalence of Anaplasma marginale in water buffaloes in Marajo Island, Brazil. Ticks Tick Borne Dis. 2014;5(6):801–4.View ArticlePubMedGoogle Scholar
  10. Quiroz-Castaneda RE, Amaro-Estrada I, Rodriguez-Camarillo SD. Anaplasma marginale: diversity, virulence, and vaccine landscape through a genomics approach. Biomed Res Int. 2016;2016:9032085.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Liu Z, Luo J, Bai Q, Ma M, Guan G, Yin H. Amplification of 16S rRNA genes of Anaplasma species in China for phylogenetic analysis. Vet Microbiol. 2005;107(1–2):145–8.View ArticlePubMedGoogle Scholar
  12. Wen BH, Cao WC, Pan H. Ehrlichiae and ehrlichial diseases in China. Ann N Y Acad Sci. 2003;990:45–53.View ArticlePubMedGoogle Scholar
  13. Zhang LM, Wang Y, Cai DJ, He GM, Cheng ZQ, Liu JZ, et al. Detection of Anaplasma marginale in Hyalomma asiaticum ticks by PCR assay. Parasitol Res. 2013;112(7):2697–702.View ArticlePubMedGoogle Scholar
  14. Qiu HX, Kelly PJ, Zhang JL, Luo QH, Yang Y, Mao YJ, et al. Molecular detection of Anaplasma spp. and Ehrlichia spp. in ruminants from twelve provinces of China. Can J Infect Dis Med. 2016;2016:9183861.Google Scholar
  15. Zhou ZY, Nie K, Tang C, Wang ZY, Zhou RQ, SJ H, et al. Phylogenetic analysis of the genus Anaplasma in southwestern China based on 16S rRNA sequence. Res Vet Sci. 2010;89(2):262–5.View ArticlePubMedGoogle Scholar
  16. Torina A, Agnone A, Blanda V, Alongi A, D'Agostino R, Caracappa S, et al. Development and validation of two PCR tests for the detection of and differentiation between Anaplasma ovis and Anaplasma marginale. Ticks Tick Borne Dis. 2012;3(5–6):282–6.Google Scholar
  17. de la Fuente J, Atkinson MW, Naranjo V, de Mera IGF, Mangold AJ, Keating KA, et al. Sequence analysis of the msp4 gene of Anaplasma ovis strains. Vet Microbiol. 2007;119(2–4):375–81.View ArticlePubMedGoogle Scholar
  18. Lew AE, Bock RE, Minchin CM, Masaka SA. msp1 alpha polymerase chain reaction assay for specific detection and differentiation of Anaplasma marginale isolates. Vet Microbiol. 2002;87(4):325–35.View ArticleGoogle Scholar
  19. Almazan C, Medrano C, Ortiz M, de la Fuente J. Genetic diversity of Anaplasma marginale strains from an outbreak of bovine anaplasmosis in an endemic area. Vet Parasitol. 2008;158(1–2):103–9.View ArticlePubMedGoogle Scholar
  20. George N, Bhandari V, Sharma P. Phylogenetic relationship and genotypic variability in Anaplasma marginale strains causing anaplasmosis in India. Infect Genet Evol. 2017;48:71–5.View ArticlePubMedGoogle Scholar
  21. Catanese HN, Brayton KA, Gebremedhin AH. RepeatAnalyzer: a tool for analysing and managing short-sequence repeat data. BMC Genomics. 2016;17:422.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Kocan KM, de la Fuente J, Blouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol. 2010;167(2–4):95–107.View ArticlePubMedGoogle Scholar
  23. Reinbold JB, Coetzee JF, Hollis LC, Nickell JS, Riegel C, Olson KC, et al. The efficacy of three chlortetracycline regimens in the treatment of persistent Anaplasma marginale infection. Vet Microbiol. 2010;145(1–2):69–75.View ArticlePubMedGoogle Scholar
  24. XB W, Na RH, Wei SS, Zhu JS, Peng HJ. Distribution of tick-borne diseases in China. Parasit Vectors. 2013;6:119.View ArticleGoogle Scholar
  25. Brayton KA, Kappmeyer LS, Herndon DR, Dark MJ, Tibbals DL, Palmer GH, et al. Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proc Natl Acad Sci USA. 2005;102(3):844–9.Google Scholar
  26. Macmillan H, Brayton KA, Palmer GH, McGuire TC, Munske G, Siems WF, et al. Analysis of the Anaplasma marginale major surface protein 1 complex protein composition by tandem mass spectrometry. J Bacteriol. 2006;188(13):4983–91.View ArticlePubMedPubMed CentralGoogle Scholar
  27. de la Fuente J, Van Den Bussche RA, Garcia-Garcia JC, Rodriguez SD, Garcia MA, Guglielmone AA, et al. Phylogeography of new world isolates of Anaplasma marginale based on major surface protein sequences. Vet Microbiol. 2002;88(3):275–85.View ArticlePubMedGoogle Scholar
  28. de la Fuente J, Lew A, Lutz H, Meli ML, Hofmann-Lehmann R, Shkap V, et al. Genetic diversity of Anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development. Anim Health Res Rev. 2005;6(1):75–89.View ArticlePubMedGoogle Scholar
  29. Cabezas-Cruz A, de la Fuente J. Anaplasma marginale major surface protein 1a: a marker of strain diversity with implications for control of bovine anaplasmosis. Ticks Tick Borne Dis. 2015;6(3):205–210.Google Scholar
  30. Cabezas-Cruz A, Passos LM, Lis K, Kenneil R, Valdes JJ, Ferrolho J, et al. Functional and immunological relevance of Anaplasma marginale major surface protein 1a sequence and structural analysis. PLoS One. 2013;8(6):e65243.View ArticlePubMedPubMed CentralGoogle Scholar
  31. de la Fuente J, Garcia-Garcia JC, Blouin EF, Saliki JT, Kocan KM. Infection of tick cells and bovine erythrocytes with one genotype of the intracellular ehrlichia Anaplasma marginale excludes infection with other genotypes. Clin Diagn Lab Immun. 2002;9(3):658–668.Google Scholar
  32. de la Fuente J, Blouin EF, Kocan KM. Infection exclusion of the rickettsial pathogen Anaplasma marginale in the tick vector Dermacentor variabilis. Clin Diagn Lab Immun 2003;10(1):182–184.Google Scholar
  33. Azad AF, Beard CB. Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis. 1998;4(2):179–86.View ArticlePubMedPubMed CentralGoogle Scholar
  34. Castaneda-Ortiz EJ, Ueti MW, Camacho-Nuez M, Mosqueda JJ, Mousel MR, Johnson WC, et al. Association of Anaplasma marginale strain superinfection with infection prevalence within tropical regions. PLoS One. 2015;10(3):e0120748.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Guillemi EC, Ruybal P, Lia V, Gonzalez S, Lew S, Zimmer P, et al. Development of a multilocus sequence typing scheme for the study of anaplasma marginale population structure over space and time. Infect Genet Evol. 2015;30:186–94.View ArticlePubMedGoogle Scholar
  36. Vallejo Esquerra E, Herndon DR, Alpirez Mendoza F, Mosqueda J, Palmer GH. Anaplasma marginale superinfection attributable to pathogen strains with distinct genomic backgrounds. Infect Immun. 2014;82(12):5286–92.View ArticlePubMedPubMed CentralGoogle Scholar
  37. Palmer GH, Knowles DP, Rodriguez JL, Gnad DP, Hollis LC, Marston T, et al. Stochastic transmission of multiple genotypically distinct Anaplasma marginale strains in a herd with high prevalence of Anaplasma infection. J Clin Microbiol. 2004;42(11):5381–4.View ArticlePubMedPubMed CentralGoogle Scholar
  38. Khumalo ZTH, Catanese HN, Liesching N, Hove P, Collins NE, Chaisi ME, et al. Characterization of Anaplasma marginale subsp. centrale strains by use of msp1aS genotyping reveals a wildlife reservoir. J Clin Microbiol. 2016;54(10):2503–12.Google Scholar

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