Spatial distance between sites of sampling associated with genetic variation among Neospora caninum in aborted bovine foetuses from northern Italy.
Abortion, Veterinary
/ parasitology
Animals
Antibodies, Protozoan
/ blood
Cattle
Cattle Diseases
/ parasitology
Coccidiosis
/ epidemiology
DNA Fingerprinting
DNA Mutational Analysis
Farms
/ statistics & numerical data
Female
Fetus
/ parasitology
Genetic Variation
Genotype
Geography
Italy
/ epidemiology
Microsatellite Repeats
/ genetics
Neospora
/ classification
Pregnancy
Sampling Studies
Bovine abortion
Holstein friesian cattle
Italy
Microsatellite typing
Multilocus genotyping
Neosporosis
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
13 Jan 2021
13 Jan 2021
Historique:
received:
02
10
2020
accepted:
16
12
2020
entrez:
14
1
2021
pubmed:
15
1
2021
medline:
24
7
2021
Statut:
epublish
Résumé
Neospora caninum, a coccidian protozoan, represents an important cause of bovine abortion. Available N. caninum strains show considerable variation in vitro and in vivo, including different virulence in cattle. To which extent sexual recombination, which is possible in the intestines of domestic dogs and closely related carnivores as definitive hosts, contributes to this variation is not clear yet. Aborted bovine foetuses were collected between 2015 and early 2019 from Italian Holstein Friesian dairy herds suffering from reproductive problems. A total of 198 samples were collected from 165 intensive farms located in Lombardy, northern Italy. N. caninum samples were subjected to multilocus-microsatellite genotyping using ten previously established microsatellite markers. In addition to our own data, those from a recent study providing data on five markers from other northern Italian regions were included and analysed. Of the 55 samples finally subjected to genotyping, 35 were typed at all or 9 out of 10 loci and their individual multilocus-microsatellite genotype (MLMG) determined. Linear regression revealed a statistically significant association between the spatial distance of the sampling sites with the genetic distance of N. caninum MLMGs (P < 0.001). Including data from this and a previous North Italian study into eBURST analysis revealed that several of N. caninum MLMGs from northern Italy separate into four groups; most of the samples from Lombardy clustered in one of these groups. Principle component analysis revealed similar clusters and confirmed MLMG groups identified by eBURST. Variations observed between MLMGs were not equally distributed over all loci, but predominantly observed in MS7, MS6A, or MS10. Our findings confirm the concept of local N. caninum subpopulations. The geographic distance of sampling was associated with the genetic distance as determined by microsatellite typing. Results suggest that multi-parental recombination in N. caninum is a rare event, but does not exclude uniparental mating. More comprehensive studies on microsatellites in N. caninum and related species like Toxoplasma gondii should be undertaken, not only to improve genotyping capabilities, but also to understand possible functions of these regions in the genomes of these parasites.
Sections du résumé
BACKGROUND
BACKGROUND
Neospora caninum, a coccidian protozoan, represents an important cause of bovine abortion. Available N. caninum strains show considerable variation in vitro and in vivo, including different virulence in cattle. To which extent sexual recombination, which is possible in the intestines of domestic dogs and closely related carnivores as definitive hosts, contributes to this variation is not clear yet.
METHODS
METHODS
Aborted bovine foetuses were collected between 2015 and early 2019 from Italian Holstein Friesian dairy herds suffering from reproductive problems. A total of 198 samples were collected from 165 intensive farms located in Lombardy, northern Italy. N. caninum samples were subjected to multilocus-microsatellite genotyping using ten previously established microsatellite markers. In addition to our own data, those from a recent study providing data on five markers from other northern Italian regions were included and analysed.
RESULTS
RESULTS
Of the 55 samples finally subjected to genotyping, 35 were typed at all or 9 out of 10 loci and their individual multilocus-microsatellite genotype (MLMG) determined. Linear regression revealed a statistically significant association between the spatial distance of the sampling sites with the genetic distance of N. caninum MLMGs (P < 0.001). Including data from this and a previous North Italian study into eBURST analysis revealed that several of N. caninum MLMGs from northern Italy separate into four groups; most of the samples from Lombardy clustered in one of these groups. Principle component analysis revealed similar clusters and confirmed MLMG groups identified by eBURST. Variations observed between MLMGs were not equally distributed over all loci, but predominantly observed in MS7, MS6A, or MS10.
CONCLUSIONS
CONCLUSIONS
Our findings confirm the concept of local N. caninum subpopulations. The geographic distance of sampling was associated with the genetic distance as determined by microsatellite typing. Results suggest that multi-parental recombination in N. caninum is a rare event, but does not exclude uniparental mating. More comprehensive studies on microsatellites in N. caninum and related species like Toxoplasma gondii should be undertaken, not only to improve genotyping capabilities, but also to understand possible functions of these regions in the genomes of these parasites.
Identifiants
pubmed: 33441141
doi: 10.1186/s13071-020-04557-6
pii: 10.1186/s13071-020-04557-6
pmc: PMC7805081
doi:
Substances chimiques
Antibodies, Protozoan
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
47Subventions
Organisme : Deutscher Akademischer Austauschdienst
ID : 57440917
Références
Dubey JP, Hemphill A, Calero-Bernal R, Schares G. Neosporosis in animals. Boca Rotan: CRC Press; 2017.
doi: 10.1201/9781315152561
Dubey JP, Schares G, Ortega-Mora LM. Epidemiology and control of neosporosis and Neospora caninum. Clin Microbiol Rev. 2007;20:323–67.
pubmed: 17428888
pmcid: 1865591
doi: 10.1128/CMR.00031-06
Dubey JP, Jenkins MC, Rajendran C, Miska K, Ferreira LR, Martins J, et al. Gray wolf (Canis lupus) is a natural definitive host for Neospora caninum. Vet Parasitol. 2011;181:382–7.
pubmed: 21640485
doi: 10.1016/j.vetpar.2011.05.018
Gondim LF, McAllister MM, Pitt WC, Zemlicka DE. Coyotes (Canis latrans) are definitive hosts of Neospora caninum. Int J Parasitol. 2004;34:159–61.
pubmed: 15037103
doi: 10.1016/j.ijpara.2004.01.001
King JS, Slapeta J, Jenkins DJ, Al-Qassab SE, Ellis JT, Windsor PA. Australian dingoes are definitive hosts of Neospora caninum. Int J Parasitol. 2010;40:945–50.
pubmed: 20149793
doi: 10.1016/j.ijpara.2010.01.008
Trees AJ, Williams DJ. Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii. Trends Parasitol. 2005;21:558–61.
pubmed: 16223599
doi: 10.1016/j.pt.2005.09.005
McCann CM, McAllister MM, Gondim LF, Smith RF, Cripps PJ, Kipar A, et al. Neospora caninum in cattle: experimental infection with oocysts can result in exogenous transplacental infection, but not endogenous transplacental infection in the subsequent pregnancy. Int J Parasitol. 2007;37:1631–9.
pubmed: 17624353
doi: 10.1016/j.ijpara.2007.05.012
McAllister MM, Wallace RL, Björkman C, Gao L, Firkins LD. A probable source of Neospora caninum infection in an abortion outbreak in dairy cows. Bovine Pract. 2005;39:69–74.
Schares G, Bärwald A, Staubach C, Söndgen P, Rauser M, Schröder R, et al. p38-avidity-ELISA: examination of herds experiencing epidemic or endemic Neospora caninum-associated bovine abortion. Vet Parasitol. 2002;106:293–305.
pubmed: 12079735
doi: 10.1016/S0304-4017(02)00103-6
Basso W, Schares S, Minke L, Bärwald A, Maksimov A, Peters M, et al. Microsatellite typing and avidity analysis suggest a common source of infection in herds with epidemic Neospora caninum-associated bovine abortion. Vet Parasitol. 2010;173:24–31.
pubmed: 20609521
doi: 10.1016/j.vetpar.2010.06.009
Khan A, Fujita AW, Randle N, Regidor-Cerrillo J, Shaik JS, Shen K, et al. Global selective sweep of a highly inbred genome of the cattle parasite Neospora caninum. Proc Natl Acad Sci USA. 2019;116:22764–73.
pubmed: 31636194
pmcid: 6842595
doi: 10.1073/pnas.1913531116
Calarco L, Barratt J, Ellis J. Genome wide Identification of mutational hotspots in the apicomplexan parasite Neospora caninum and the implications for virulence. Genome Biol Evol. 2018;10:2417–31.
pubmed: 30165699
pmcid: 6147731
doi: 10.1093/gbe/evy188
Felius M, Beerling M-L, Buchanan DS, Theunissen B, Koolmees PA, Lenstra JA. On the history of cattle genetic resources. Diversity. 2014;6:705–50.
doi: 10.3390/d6040705
Regidor-Cerrillo J, Gomez-Bautista M, Sodupe I, Aduriz G, Alvarez-Garcia G, Del PI, et al. In vitro invasion efficiency and intracellular proliferation rate comprise virulence-related phenotypic traits of Neospora caninum. Vet Res. 2011;42:41.
pubmed: 21345202
pmcid: 3052184
doi: 10.1186/1297-9716-42-41
Dellarupe A, Regidor-Cerrillo J, Jimenez-Ruiz E, Schares G, Unzaga JM, Venturini MC, et al. Comparison of host cell invasion and proliferation among Neospora caninum isolates obtained from oocysts and from clinical cases of naturally infected dogs. Exp Parasitol. 2014;145:22–8.
pubmed: 25045851
doi: 10.1016/j.exppara.2014.07.003
Jimenez-Pelayo L, Garcia-Sanchez M, Regidor-Cerrillo J, Horcajo P, Collantes-Fernandez E, Gomez-Bautista M, et al. Differential susceptibility of bovine caruncular and trophoblast cell lines to infection with high and low virulence isolates of Neospora caninum. Parasites Vect. 2017;10:463.
doi: 10.1186/s13071-017-2409-9
Rojo-Montejo S, Collantes-Fernandez E, Regidor-Cerrillo J, Alvarez-Garcia G, Marugan-Hernandez V, Pedraza-Diaz S, et al. Isolation and characterization of a bovine isolate of Neospora caninum with low virulence. Vet Parasitol. 2009;159:7–16.
pubmed: 19027235
doi: 10.1016/j.vetpar.2008.10.009
Regidor-Cerrillo J, Gomez-Bautista M, Del PI, Jimenez-Ruiz E, Aduriz G, Ortega-Mora LM. Influence of Neospora caninum intra-specific variability in the outcome of infection in a pregnant BALB/c mouse model. Vet Res. 2010;41:52.
pubmed: 20416260
pmcid: 2878169
doi: 10.1051/vetres/2010024
Dellarupe A, Regidor-Cerrillo J, Jimenez-Ruiz E, Schares G, Unzaga JM, Venturini MC, et al. Clinical outcome and vertical transmission variability among canine Neospora caninum isolates in a pregnant mouse model of infection. Parasitology. 2014;141:356–66.
pubmed: 24148606
doi: 10.1017/S0031182013001479
Rojo-Montejo S, Collantes-Fernandez E, Blanco-Murcia J, Rodriguez-Bertos A, Risco-Castillo V, Ortega-Mora LM. Experimental infection with a low virulence isolate of Neospora caninum at 70 days gestation in cattle did not result in foetopathy. Vet Res. 2009;40:5.
doi: 10.1051/vetres/2009032
Chryssafidis AL, Canton G, Chianini F, Innes EA, Madureira EH, Gennari SM. Pathogenicity of Nc-Bahia and Nc-1 strains of Neospora caninum in experimentally infected cows and buffaloes in early pregnancy. Parasitol Res. 2014;113:1521–8.
pubmed: 24562816
doi: 10.1007/s00436-014-3796-x
Regidor-Cerrillo J, Arranz-Solis D, Benavides J, Gomez-Bautista M, Castro-Hermida JA, Mezo M, et al. Neospora caninum infection during early pregnancy in cattle: how the isolate influences infection dynamics, clinical outcome and peripheral and local immune responses. Vet Res. 2014;45:10.
pubmed: 24479988
pmcid: 3922688
doi: 10.1186/1297-9716-45-10
Jimenez-Pelayo L, Garcia-Sanchez M, Vazquez P, Regidor-Cerrillo J, Horcajo P, Collantes-Fernandez E, et al. Early Neospora caninum infection dynamics in cattle after inoculation at mid-gestation with high (Nc-Spain7)- or low (Nc-Spain1H)-virulence isolates. Vet Res. 2019;50:1.
doi: 10.1186/s13567-019-0691-6
Regidor-Cerrillo J, Pedraza-Diaz S, Gomez-Bautista M, Ortega-Mora LM. Multilocus microsatellite analysis reveals extensive genetic diversity in Neospora caninum. J Parasitol. 2006;92:517–24.
pubmed: 16883994
doi: 10.1645/GE-713R.1
Zucali M, Tamburini A, Sandrucci A, Bava L. Global warming and mitigation potential of milk and meat production in Lombardy (Italy). J Clean Prod. 2017;153:474–82.
doi: 10.1016/j.jclepro.2016.11.037
Otranto D, Llazari A, Testini G, Traversa D, di Regalbono AF, Badan M, et al. Seroprevalence and associated risk factors of neosporosis in beef and dairy cattle in Italy. Vet Parasitol. 2003;118:7–18.
pubmed: 14651870
doi: 10.1016/j.vetpar.2003.10.008
Sala G, Gazzonis A, Boccardo A, Coppoletta E, Galasso C, Manfredi MT, et al. Using beef-breed semen in seropositive dams for the control of bovine neosporosis. Prev Vet Med. 2018;161:127–33.
pubmed: 30466653
doi: 10.1016/j.prevetmed.2018.10.024
Regidor-Cerrillo J, Diez-Fuertes F, Garcia-Culebras A, Moore DP, Gonzalez-Warleta M, Cuevas C, et al. Genetic diversity and geographic population structure of bovine Neospora caninum determined by microsatellite genotyping analysis. PLoS ONE. 2013;8:e72678.
pubmed: 23940816
pmcid: 3735528
doi: 10.1371/journal.pone.0072678
Cabrera A, Fresia P, Berna L, Silveira C, Macias-Rioseco M, Arevalo AP, et al. Isolation and molecular characterization of four novel Neospora caninum strains. Parasitol Res. 2019;118:3535–42.
pubmed: 31701296
doi: 10.1007/s00436-019-06474-9
Pedraza-Diaz S, Marugan-Hernandez V, Collantes-Fernandez E, Regidor-Cerrillo J, Rojo-Montejo S, Gomez-Bautista M, et al. Microsatellite markers for the molecular characterization of Neospora caninum: application to clinical samples. Vet Parasitol. 2009;166:38–46.
pubmed: 19720464
doi: 10.1016/j.vetpar.2009.07.043
Regidor-Cerrillo J, Horcajo P, Ceglie L, Schiavon E, Ortega-Mora LM, Natale A. Genetic characterization of Neospora caninum from Northern Italian cattle reveals high diversity in European N. caninum populations. Parasitol Res. 2020;119:1353–62.
pubmed: 32157394
doi: 10.1007/s00436-020-06642-2
Constantin EM, Schares G, Grossmann E, Sauter K, Romig T, Hartmann S. Untersuchungen zur Rolle des Rotfuchses (Vulpes vulpes) als möglicher Endwirt von Neospora caninum. Berl Munch Tierarztl Wochenschr. 2011;124:148–53.
pubmed: 21465771
Legnani S, Pantchev N, Forlani A, Zini E, Schares G, Balzer J, et al. Emergence of cutaneous neosporosis in a dog receiving immunosuppressive therapy: molecular identification and management. Vet Dermatol. 2016;27:49-e14.
pubmed: 26627466
doi: 10.1111/vde.12273
Dubey JP, Hattel AL, Lindsay DS, Topper MJ. Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. J Am Vet Med Assoc. 1988;193:1259–63.
pubmed: 3144521
Basso W, Schares S, Barwald A, Herrmann DC, Conraths FJ, Pantchev N, et al. Molecular comparison of Neospora caninum oocyst isolates from naturally infected dogs with cell culture-derived tachyzoites of the same isolates using nested polymerase chain reaction to amplify microsatellite markers. Vet Parasitol. 2009;160:43–50.
pubmed: 19084341
doi: 10.1016/j.vetpar.2008.10.085
Dubey JP, Dorough KR, Jenkins MC, Liddell S, Speer CA, Kwok OCH, et al. Canine neosporosis: clinical signs, diagnosis, treatment and isolation of Neospora caninum in mice and cell culture. Int J Parasitol. 1998;28:1293–304.
pubmed: 9762578
doi: 10.1016/S0020-7519(98)00099-X
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B (Methodol). 1995;57:289–300.
Bruvo R, Michiels NK, D’Souza TG, Schulenburg H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol. 2004;13:2101–6.
pubmed: 15189230
doi: 10.1111/j.1365-294X.2004.02209.x
Kamvar ZN, Tabima JF, Grunwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281.
pubmed: 24688859
pmcid: 3961149
doi: 10.7717/peerj.281
Haubold B, Hudson RR. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics. 2000;16:847–9.
pubmed: 11108709
doi: 10.1093/bioinformatics/16.9.847
Goudet J. HierFstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes. 2005;5:184–6.
doi: 10.1111/j.1471-8286.2004.00828.x
de Meeûs T, Goudet J. A step-by-step tutorial to use HierFstat to analyse populations hierarchically structured at multiple levels. Infect Genet Evol. 2007;7:731–5.
pubmed: 17765664
doi: 10.1016/j.meegid.2007.07.005
Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol. 2004;186:1518–30.
pubmed: 14973027
pmcid: 344416
doi: 10.1128/JB.186.5.1518-1530.2004
Dubey JP, Schares G. Diagnosis of bovine neosporosis. Vet Parasitol. 2006;140:1–34.
pubmed: 16730126
doi: 10.1016/j.vetpar.2006.03.035
Mancini G, Gargani M, Chillemi G, Nicolazzi EL, Marsan PA, Valentini A, et al. Signatures of selection in five Italian cattle breeds detected by a 54K SNP panel. Mol Biol Rep. 2014;41:957–65.
pubmed: 24442315
pmcid: 3929051
doi: 10.1007/s11033-013-2940-5
Buchanan DS. Breeds of dairy cattle (major Bos taurus breeds). In: Reference module in food science. The Netherlands: Elsevier; 2016.
Schlötterer C, Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 1992;20:211–5.
pubmed: 1741246
pmcid: 310356
doi: 10.1093/nar/20.2.211
Viguera E, Canceill D, Ehrlich SD. Replication slippage involves DNA polymerase pausing and dissociation. EMBO J. 2001;20:2587–95.
pubmed: 11350948
pmcid: 125466
doi: 10.1093/emboj/20.10.2587
Ellegren H. Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet. 2000;16:551–8.
pubmed: 11102705
doi: 10.1016/S0168-9525(00)02139-9
Schlötterer C. Evolutionary dynamics of microsatellite DNA. Chromosoma. 2000;109:365–71.
pubmed: 11072791
doi: 10.1007/s004120000089
Estoup A, Jarne P, Cornuet JM. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol. 2002;11:1591–604.
pubmed: 12207711
doi: 10.1046/j.1365-294X.2002.01576.x
Bagshaw ATM. Functional mechanisms of microsatellite DNA in eukaryotic genomes. Genome Biol Evol. 2017;9:2428–43.
pubmed: 28957459
pmcid: 5622345
doi: 10.1093/gbe/evx164
Mathema VB, Nakeesathit S, White NJ, Dondorp AM, Imwong M. Genome-wide microsatellite characteristics of five human Plasmodium species, focusing on Plasmodium malariae and P. ovale curtisi. Parasite. 2020;27:34.
pubmed: 32410726
pmcid: 7227371
doi: 10.1051/parasite/2020034
Dubey JP, Schares G. Neosporosis in animals—the last five years. Vet Parasitol. 2011;180:90–108.
pubmed: 21704458
doi: 10.1016/j.vetpar.2011.05.031
Roman LRS, Horcajo P, Regidor-Cerrillo J, Fernandez-Escobar M, Collantes-Fernandez E, Gutierrez-Blazquez D, et al. Comparative tachyzoite proteome analyses among six Neospora caninum isolates with different virulence. Int J Parasitol. 2020;50:377–88.
doi: 10.1016/j.ijpara.2020.02.003
Ajzenberg D, Collinet F, Aubert D, Villena I, Darde ML, French ToxoBs network g, et al. The rural-urban effect on spatial genetic structure of type II Toxoplasma gondii strains involved in human congenital toxoplasmosis, France 2002–2009. Infect Genet Evol. 2015;36:511–6.
pubmed: 26305624
doi: 10.1016/j.meegid.2015.08.025