Phylogeographic analysis reveals association of tick-borne pathogen, Anaplasma marginale, MSP1a sequences with ecological traits affecting tick vector performance

BMC Biology

Volumn 7, Issue , 2009, Pages 57-

  Estrada Peña, Agustín ^a   Naranjo, Victoria ^b,c   Acevedo Whitehouse, Karina ^d   Mangold, Atilio J ^e   Kocan, Katherine M ^c   de la Fuente, José ^b,c  

^a UNIVERSIDAD DE ZARAGOZA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^c OKLAHOMA STATE UNIVERSITY   (United States)

^d INSTITUTE OF ZOOLOGY   (United Kingdom)

^e INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MAJOR SURFACE PROTEIN 1A; PROTEIN MSP 1A; UNCLASSIFIED DRUG; MAJOR SURFACE PROTEIN 1A, ANAPLASMA; MESSENGER RNA; MICROSATELLITE DNA; OUTER MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; ANAPLASMA MARGINALE; ARTICLE; BACTERIAL STRAIN; BIOGEOGRAPHIC REGION; CONTROLLED STUDY; ECOLOGICAL GENETICS; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; MICROSATELLITE MARKER; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE TRANSMISSION; PHYLOGENY; PHYLOGEOGRAPHY; STRAIN IDENTIFICATION; TICK; ANALYSIS OF VARIANCE; ANAPLASMOSIS; ANIMAL; CATTLE; CATTLE DISEASE; CHEMISTRY; CONSENSUS SEQUENCE; DISEASE TRANSMISSION; GENETIC SELECTION; GENETICS; GENOTYPE; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; NONPARAMETRIC TEST; PARASITE VECTOR; PATHOGENICITY; RHIPICEPHALUS; SEASON; SEQUENCE HOMOLOGY; TOPOGRAPHY;

ANAPLASMA; ANAPLASMA MARGINALE; ANAPLASMATACEAE; BOOPHILUS; IXODIDA; RHIPICEPHALUS; RICKETTSIALES;

AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANAPLASMA MARGINALE; ANAPLASMOSIS; ANIMALS; ARACHNID VECTORS; BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; CATTLE; CATTLE DISEASES; CONSENSUS SEQUENCE; EVOLUTION, MOLECULAR; GENOTYPE; MICROSATELLITE REPEATS; PHYLOGENY; REPETITIVE SEQUENCES, AMINO ACID; RHIPICEPHALUS; RNA, MESSENGER; SEASONS; SELECTION (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID; STATISTICS, NONPARAMETRIC; TOPOGRAPHY, MEDICAL;

EID: 70350008244     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-7-57     Document Type: Article

References (49)

1. Dumler JS, Barbet AC, Bekker CPJ, Dasch GA, Palmer GH, Ray SC, Rikihisa Y, Rurangirwa FR. Reorganization of the 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 subjective synonyms of Ehrlichia phagocytophila. Int J Sys Evol Microbiol 2001, 51:2145-2165.
2. Kocan KM, de la Fuente J, Blouin EF, Garcia-Garcia JC. Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitol 2004, 129:S285-S300.
3. Kocan KM, de la Fuente J, Blouin EF. Advances toward understanding the molecular biology of the Anaplasma-tick interface. Front Biosci 2008, 13:7032-7045. 10.2741/3208, 18508714.
4. Estrada-Peña A, Bouattour A, Camicas JL, Guglielmone A, Horak I, Jongejan F, Latif A, Pegram R, Walker AR. The known distribution and ecological preferences of the tick subgenus Boophilus (Acari: Ixodidae) in Africa and Latin America. Exp Appl Acarol 2006, 38:219-235. 10.1007/s10493-006-0003-5, 16596355.
5. de la Fuente J, Kocan KM, Blouin EF, Zivkovic Z, Naranjo V, Almazán C, Esteves E, Jongejan J, Daffre S, Mangold AJ. Functional genomics and evolution of tick-Anaplasma interactions and vaccine development. Vet Parasitol 2009,
6. de la Fuente J, Garcia-Garcia JC, Blouin EF, Rodríguez SD, Garcia MA, Kocan KM. Evolution and function of tandem repeats in the major surface protein 1a of the ehrlichial pathogen Anaplasma marginale. Anim Health Res Rev 2001, 2:163-173.
7. de la Fuente J, Lew A, Lutz H, Meli ML, Hofmann-Lehmann R, Shkap V, Molad T, Mangold AJ, Almazán C, Naranjo V, Gortázar C, Torina A, Caracappa S, García-Pérez AL, Barral M, Oporto B, Ceci L, Carelli G, Blouin EF, Kocan KM. Genetic diversity of Anaplasma species major surface proteins and implications for anaplasmosis serodiagnosis and vaccine development. Anim Health Res Rev 2005, 6:75-89. 10.1079/AHR2005104, 16164010.
8. Brayton KA, Kappmeyer LS, Herndon DR, Dark MJ, Tibbals DL, Palmer GH, McGuire TC, Knowles DP. 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, 102:844-849. 10.1073/pnas.0406656102, 545514, 15618402.
9. Dunning Hotopp JC, Lin M, Madupu R, Crabtree J, Angiuoli SV, Eisen J, Seshadri R, Ren Q, Wu M, Utterback TR, Smith S, Lewis M, Khouri H, Zhang C, Niu H, Lin Q, Ohashi N, Zhi N, Nelson W, Brinkac LM, Dodson RJ, Rosovitz MJ, Sundaram J, Daugherty SC, Davidsen T, Durkin AS, Gwinn M, Haft DH, Selengut JD, Sullivan SA. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2006, 2:e21. 10.1371/journal.pgen.0020021, 1366493,1366493, 16482227.
10. Allred DR, McGuire TC, Palmer GH, Leib SR, Harkins TM, McElwain TF, Barbet AF. Molecular basis for surface antigen size polymorphisms and conservation of a neutralization-sensitive epitope in Anaplasma marginale. Proc Natl Acad Sci USA 1990, 87:3220-3224. 10.1073/pnas.87.8.3220, 53867, 1691504.
11. de la Fuente J, Ruybal P, Mtshali MS, Naranjo V, Shuqing L, Mangold AJ, Rodríguez SD, Jiménez R, Vicente J, Moretta R, Torina A, Almazán C, Mbati PM, Torioni de Echaide S, Farber M, Rosario-Cruz R, Gortazar C, Kocan KM. Analysis of world strains of Anaplasma marginale using major surface protein 1a repeat sequences. Vet Microbiol 2007, 119:382-390. 10.1016/j.vetmic.2006.09.015, 17084044.
12. McGarey DJ, Allred DR. Characterization of hemagglutinating components on the Anaplasma marginale initial body surface and identification of possible adhesins. Infect Immun 1994, 62:4587-4593. 303147, 7927725.
13. McGarey DJ, Barbet AF, Palmer GH, McGuire TC, Allred DR. Putative adhesins of Anaplasma marginale: major surface polypeptides 1a and 1b. Infect Immun 1994, 62:4594-4601. 303148, 7927726.
14. de la Fuente J, Garcia-Garcia JC, Blouin EF, Kocan KM. Differential adhesion of major surface proteins 1a and 1b of the ehrlichial cattle pathogen Anaplasma marginale to bovine erythrocytes and tick cells. Int J Parasitol 2001, 31:145-153. 10.1016/S0020-7519(00)00162-4, 11239934.
15. de la Fuente J, Blouin EF, Manzano-Roman R, Naranjo V, Almazán C, Pérez de la Lastra JM, Zivkovic Z, Jongejan F, Kocan KM. Functional genomic studies of tick cells in response to infection with the cattle pathogen, Anaplasma marginale. Genomics 2007, 90:712-722. 10.1016/j.ygeno.2007.08.009, 17964755.
16. de la Fuente J, García-García 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 Immunol 2002, 9:658-668. 119989, 11986275.
17. 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 Immunol 2003, 10:182-184. 145288, 12522060.
18. Palmer GH, Knowles DP, Rodriguez JL, Gnad DP, Hollis LC, Marston T, Brayton KA. Stochastic transmission of multiple genotypically distinct Anaplasma marginale strains in a herd with high prevalence of Anaplasma infection. J Clin Microbiol 2004, 42:5381-5384. 10.1128/JCM.42.11.5381-5384.2004, 525272, 15528749.
19. de la Fuente J, Bussche RA, Prado T, Kocan KM. Anaplasma marginale major surface protein 1α genotypes evolved under positive selection pressure but are not markers for geographic strains. J Clin Microbiol 2003, 41:1609-1616. 10.1128/JCM.41.4.1609-1616.2003, 153873, 12682152.
20. de la Fuente J, Bussche RA, Kocan KM. Molecular phylogeny and biogeography of North American strains of Anaplasma marginale (Rickettsiaceae: Ehrlichieae). Vet Parasitol 2001, 97:65-76. 10.1016/S0304-4017(01)00378-8, 11337128.
21. Genbank sequence database. , http://www.ncbi.nlm.nih.gov/
22. Hargrove WW, Hoffman FM. Potential of multivariate quantitative methods for delineation and visualization of ecoregions. Environ Manage 2004, 34(Suppl 1):S39-S60. 10.1007/s00267-003-1084-0, 15883870.
23. Estrada-Peña A, Thuiller W. An assessment of the effect of data partitioning on the performance of modelling algorithms for habitat suitability for ticks. Med Vet Entomol 2008, 22:248-257. 10.1111/j.1365-2915.2008.00745.x, 18816273.
24. Eastman JR, Fulk M. Long sequence time series evaluation using standardized principal components. Photogrammetric Engineer Rem Sens 1993, 59:991-996.
25. De'Ath G. Multivariate regression trees: a new technique for modeling species-environment relationships. Ecology 2002, 83:1105-1007.
26. Dufrêne M, Legendre P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 1997, 67:345-366.
27. Kumar S, Dudley J, Nei M, Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9:299-306. 10.1093/bib/bbn017, 2562624, 18417537.
28. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
29. Jukes TH, Cantor CR. Evolution of protein molecules. Mammalian protein metabolism 1969, 21-132. New York, Academic Press, Inc, Munro HN.
30. Legendre P, Fortin M. Spatial pattern and ecological analysis. Vegetation 1989, 80:107-138.
31. Excoffier L, Smouse P, Quattro J. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 1992, 131:479-491. 1205020, 1644282.
32. Excoffier L, Laval G, Schneider S. Arlequin Ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
33. Guo S, Thomson E. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992, 48:361-372. 10.2307/2532296, 1637966.
34. Lee C, Lee S, Shin SG, Hwang S. Real-time PCR determination of rRNA gene copy number: absolute and relative quantification assays with Escherichia coli. Appl Microbiol Biotechnol 2008, 78:371-376. 10.1007/s00253-007-1300-6, 18074129.
35. Hume JCC, Lyons EJ, Day KP. Human migration, mosquitoes and the evolution of Plasmodium falciparum. Trends Parasitol 2003, 19:144-149. 10.1016/S1471-4922(03)00008-4, 12643998.
36. Richards CL, Carstens BC, Knowles LL. Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses. J Biogeogr 2007, 34:1833-1845.
37. Sumilo D, Bormane A, Asokliene L, Lucenko I, Vasilenko V, Randolph SE. Tick-borne encephalitis in the Baltic States: identifying risk factors in space and time. Int J Med Microbiol 2006, 296:76-79. 10.1016/j.ijmm.2005.12.006, 16530480.
38. Estrada-Peña A, Vatansever Z, Gargili A, Buzgan T. An early warning system for Crimean-Congo haemorrhagic fever seasonality in Turkey based on remote sensing technology. Geospat Health 2007, 2:127-135.
39. Scharlemann JP, Benz D, Hay SI, Purse BV, Tatem AJ, Wint GR, Rogers DJ. Global data for ecology and epidemiology: a novel algorithm for temporal Fourier processing MODIS data. PLoS ONE 2008, 9:e1408.
40. Randolph SE, Rogers DJ. Tick-borne disease systems: mapping geographic and phylogenetic space. Adv Parasitol 2006, 62:263-291. 10.1016/S0065-308X(05)62008-8, 16647973.
41. Ma J, Campbell A, Karlin S. Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. J Bacteriol 2002, 184:5733-5745. 10.1128/JB.184.20.5733-5745.2002, 139613, 12270832.
42. Garcia-Garcia JC, de la Fuente J, Blouin EF, Halbur T, Onet VC, Saliki JT, Kocan KM. Differential expression of the msp1α gene of Anaplasma marginale occurs in bovine erythrocytes and tick cells. Vet Microbiol 2004, 98:261-272. 10.1016/j.vetmic.2003.10.021, 15036535.
43. Estrada-Peña A, Corson M, Venzal JM, Mangold AJ, Guglielmone A. Changes in climate and habitat suitability for the cattle tick Boophilus microplus in its southern Neotropical distribution range. J Vector Ecol 2006, 31:158-167. 10.3376/1081-1710(2006)31[158:CICAHS]2.0.CO;2, 16859105.
44. Ivancovich JC, Braithwaite GB, Barnett S. Comportamiento de los estadios no-parasitarios de la garrapata del ganado - Boophilus microplus (Canestrini). IV. Siete diferentes localidades. Bol Ins Nac Tecnol Agropec Est Exp Reg Chaco 1984, 88:71-109.
45. Lima WS, Ribeiro MF, Guimaraes MP. Seasonal variation of Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae) in cattle in Minas Gerais State, Brazil. Trop Anim Health Prod 2000, 32:375-380. 10.1023/A:1005229602422, 11147277.
46. Guglielmone AA. The level of infestation with the vector of cattle babesiosis in Argentina. Mem Inst Oswaldo Cruz 1992, 87:133-137. 10.1590/S0074-02761992000700020, 1343682.
47. Labruna MB, Naranjo V, Mangold AJ, Thompson C, Estrada-Peña A, Guglielmone AA, Jongejan F, de la Fuente J. Allopatric speciation in ticks: genetic and reproductive divergence between geographic strains of Rhipicephalus (Boophilus) microplus. BMC Evol Biol 2009, 9:46. 10.1186/1471-2148-9-46, 2656471, 19243585.
48. Cutullé C, Jonsson NN, Seddon J. Population structure of Australian isolates of the cattle tick Rhipicephalus (Boophilus) microplus. Vet Parasitol 2009, 161:283-291. 10.1016/j.vetpar.2009.01.005, 19201542.
49. de la Fuente J, Estrada-Peña A, Venzal JM, Kocan KM, Sonenshine DE. Overview: Ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 2008, 13:6938-6946. 10.2741/3200, 18508706.