Abstract
Hemoplasma species can cause infection varying from mild to severe in a wide range of hosts, including cattle and water buffalo. Two hemoplasma species, Mycoplasma wenyonii and Candidatus Mycoplasma haemobos, have been reported in cattle and water buffalo from different parts of the world to date. There was a lack of information on the presence and distribution of these pathogens in Turkey despite the negative economic impact on livestock production. This study aimed to develop a duplex PCR assay amplifying the 16S rRNA gene, in order to analyze DNA samples obtained from 297 cattle and 360 water buffaloes, and to determine the molecular prevalence of bovine hemoplasma species in Sivas province. Bovine hemoplasma species were found in 94 of 297 (31.64%) cattle and in 17 of 360 (4.72%) water buffaloes in this study. Randomly selected six positives PCR products (three samples each species) obtained from cattle and water buffaloes were sequenced, and the consensus sequences were uploaded to GenBank. Nucleotide similarity of 96.97–100% was determined between M. wenyonii isolates obtained in this study and those of M. wenyonii isolates present in the GenBank database, whereas C. Mycoplasma haemobos isolates from this study shared 99.04–100% homology with the C. Mycoplasma haemobos isolates uploaded to the GenBank. With the current study, the molecular presence of M. wenyonii and C. Mycoplasma haemobos were documented for the first time in cattle and water buffaloes in Turkey. Considering the rate of prevalence, veterinarians should take precautions against bovine hemoplasma species to protect animal health.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this manuscript.
Code availability
Not applicable.
References
Ade J, Niethammer F, Schade B, Schilling T, Hoelzle K, Hoelzle LE (2018) Quantitative analysis of Mycoplasma wenyonii and Candidatus Mycoplasma haemobos infections in cattle using novel gapN-based realtime PCR assays. Vet Microbiol 220:1–6. https://doi.org/10.1016/j.vetmic.2018.04.028
Aktas M, Ozubek S (2017) A molecular survey of small ruminant hemotropic mycoplasmosis in Turkey, including first laboratory confirmed clinical cases caused by Mycoplasma ovis. Vet Microbiol 208:217–222. https://doi.org/10.1016/j.vetmic.2017.08.011
Altay K, Aydin MF, Dumanli N, Aktas M (2008) Molecular detection of Theileria and Babesia infections in cattle. Vet Parasitol 158(4):295–301. https://doi.org/10.1016/j.vetpar.2008.09.025
Altay K, Erol U, Sahin OF, Aytmirzakizi A (2022) First molecular detection of Anaplasma species in cattle from Kyrgyzstan; molecular identification of human pathogenic novel genotype Anaplasma capra and Anaplasma phagocytophilum related strain. Ticks Tick Borne Dis 13(1):101861. https://doi.org/10.1016/j.ttbdis.2021.101861
Altay K, Atas AD, Ograk YZ, Ozkan E (2020) Survey of Theileria, Babesia and Anaplasma Infections of Cattle and Ticks from Sivas Region of Turkey. Erciyes Üniv Vet Fak Derg 17(1): 32–38. https://doi.org/10.32707/ercivet.690618
Atas AD, Altay K, Alim A, Özkan E (2018) Survey of Dirofilaria immitis in dogs from Sivas Province in the Central Anatolia Region of Turkey. Turk J Vet Anim Sci 42(2):130–134. https://doi.org/10.3906/vet-1707-93
Ayling RD, Bisgaard-Frantzen S, Adler A, Blowey RW, Barlow AM, Millar MF, Van Der Burgt GM (2012) Detection of ‘Candidatus Mycoplasma haemobos’, Mycoplasma wenyonii and Anaplasma phagocytophilum from cattle in England. Vet Rec 170(21):543a–543a
Batista HR, Sarturi C, Stelmachtchuk FN, Oliveira DR, Morini AC, Gennari SM, Marcili A, Bastos FAN, Barata LES, Minervino AHH (2018) Prevalence and risk factors associated with ectoparasite infestation of buffaloes in an Amazonian ecosystem. Parasit Vectors 11(1):1–9. https://doi.org/10.1186/s13071-018-2917-2
Boularias G, Azzag N, Gandoin C, Bouillin C, Chomel B, Haddad N, Boulouis HJ (2020) Bovines Harbor a Diverse Array of Vector-Borne Pathogens in Northeast Algeria. Pathogens 9(11):883. https://doi.org/10.3390/pathogens9110883
de Mello VVC, de Souza Ramos IA, Herrera HM, Mendes NS, Calchi AC, Campos JBV, Macedo GC, Alves JVA, Machado RZ, Andre MR (2019) Occurrence and genetic diversity of hemoplasmas in beef cattle from the Brazilian Pantanal, an endemic area for bovine trypanosomiasis in South America. Comp Immunol Microbiol Infect Dis 66. https://doi.org/10.1016/j.cimid.2019.101337
Díaz-Sánchez AA, Corona-González B, Meli ML, Álvarez DO, Cañizares EV, Rodríguez OF, Rivero EL, Hofmann-Lehmann R (2019) First molecular evidence of bovine hemoplasma species (Mycoplasma spp.) in water buffalo and dairy cattle herds in Cuba. Parasit Vectors 12(1): 1–9. https://doi.org/10.1186/s13071-019-3325-y
Erol U, Altay K, Atas AD, Ozkan E, Sahin OF (2021) Molecular Prevalence of Canine Hepatozoonosis in Owned-Dogs in Central Part of Turkey. Isr J Vet Med 76(2):71–76
Galon EMS, Ybañez RHD, Moumouni PFA, Tumwebaze MA, Fabon RJA, Callanta MRR, Labutong KJE, Salazar GB, Liu M, Li J, Byamukama B, Li Y, Ji S, Lee SH, Ybañez AP, Claveria FC, Xuan X (2020) Molecular survey of tick-borne pathogens infecting backyard cattle and water buffaloes in Quezon province. Philippines J Vet Med Sci 82(7):886–890. https://doi.org/10.1292/jvms.19-0636
Genova SG, Streeter RN, Velguth KE, Snider TA, Kocan KM, Simpson KM (2011) Severe anemia associated with Mycoplasma wenyonii infection in a mature cow. Can Vet J 52(9):1018
Girotto-Soares A, Soares JF, Bogado ALG, de Macedo CAB, Sandeski LM, Garcia JL, Vidotto O (2016) ‘Candidatus Mycoplasma haemobos’: Transplacental transmission in dairy cows (Bos taurus). Vet Microbiol 195:22–24. https://doi.org/10.1016/j.vetmic.2016.08.020
Gonçalves LR, Teixeira MMG, Rodrigues AC, Mendes NS, Matos CA, Pereira CL, Machado RS, André MR (2018) Molecular detection of Bartonella species and haemoplasmas in wild African buffalo (Syncerus caffer) in Mozambique. Africa Parasitology Open 4(e15):1–8. https://doi.org/10.1017/pao.2018.10
Hoelzle K, Winkler M, Kramer MM, Wittenbrink MM, Dieckmann SM, Hoelzle LE (2011) Detection of Candidatus Mycoplasma haemobos in cattle with anaemia. The Vet J 187(3):408–410. https://doi.org/10.1016/j.tvjl.2010.01.016
Hofmann-Lehmann R, Meli ML, Dreher UM, Gönczi E, Deplazes P, Braun U, Engels M, Schüpbach J, Jörger K, Thoma R, Griot C, Stärk KDC, Willi B, Schmidt J, Kocan KM, Lutz H (2004) Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. J Clin Microbiol 42(8):3775–3780. https://doi.org/10.1128/JCM.42.8.3775-3780.2004
Hornok S, Meli ML, Perreten A, Farkas R, Willi B, Beugnet F, Lutz H, Hofmann-Lehmann R (2010) Molecular investigation of hard ticks (Acari: Ixodidae) and fleas (Siphonaptera: Pulicidae) as potential vectors of rickettsial and mycoplasmal agents. Vet Microbiol 140(1–2):98–104. https://doi.org/10.1016/j.vetmic.2009.07.013
Hornok S, Micsutka A, Meli ML, Lutz H, Hofmann-Lehmann R (2011) Molecular investigation of transplacental and vector-borne transmission of bovine haemoplasmas. Vet Microbiol 152(3–4):411–414. https://doi.org/10.1016/j.vetmic.2011.04.031
Inci A, Yazar S, Tuncbilek AS, Canhilal R, Doganay M, Aydın L, Aktas M, Vatansaver Z, Ozdarendeli A, Ozbel Y, Yildirim A, Duzlu O (2013) Vectors and vector-borne diseases in Turkey. Ankara Üniv Vet Fak Derg 60(4):281–296. https://doi.org/10.1501/Vetfak_0000002593
Inci A, Yildirim A, Duzlu O, Doganay M, Aksoy S (2016) Tick-borne diseases in Turkey: A review based on one health perspective. PLoS Negl Trop Dis 10(12):e0005021. https://doi.org/10.1371/journal.pntd.0005021
Jensen WA, Lappin MR, Kamkar S, Reagan WJ (2001) Use of a polymerase chain reaction assay to detect and differentiate two strains of Haemobartonella felis in naturally infected cats. Am J Vet Res 62(4):604–608. https://doi.org/10.2460/ajvr.2001.62.604
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Markoulatos P, Siafakas N, Moncany M (2002) Multiplex polymerase chain reaction: a practical approach. J Clin Lab Anal 16(1):47–51. https://doi.org/10.1002/jcla.2058
McFadden AMJ, Ha HJ, Donald JJ, Bueno IM, Van Andel M, Thompson JC, Tisdall DJ, Pulford DJ (2016) Investigation of bovine haemoplasmas and their association with anaemia in New Zealand cattle. N Z Vet J 64(1):65–68. https://doi.org/10.1080/00480169.2015.1090356
Meli ML, Willi B, Dreher UM, Cattori V, Knubben-Schweizer G, Nuss K, Braun U, Lutz H, Hofmann-Lehmann R (2010) Identification, molecular characterization, and occurrence of two bovine hemoplasma species in Swiss cattle and development of real-time TaqMan quantitative PCR assays for diagnosis of bovine hemoplasma infections. J Clin Microbiol 48(10):3563–3568. https://doi.org/10.1128/JCM.02224-09
Montes AJ, Wolfe DF, Welles EG, Tyler JW, Tepe E (1994) Infertility associated with Eperythrozoon wenyonii infection in a bull. J Am Vet Med Assoc 204(2):261–263
Neimark H, Johansson KE, Rikihisa Y, Tully JG (2001) Proposal to transfer some members of the genera Haemobartonella and Eperythrozoon to the genus Mycoplasma with descriptions of ’Candidatus Mycoplasma haemofelis’’,Candidatus Mycoplasma haemomuris’’,Candidatus Mycoplasma haemosuis’ and 'Candidatus Mycoplasma wenyonii’. Int J Syst Evol Microbiol 51(3):891–899. https://doi.org/10.1099/00207713-51-3-891
Niethammer FM, Ade J, Hoelzle LE, Schade B (2018) Hemotrophic mycoplasma in Simmental cattle in Bavaria: prevalence, blood parameters, and transplacental transmission of ‘Candidatus Mycoplasma haemobos’ and Mycoplasma wenyonii. Acta Vet Scand 60(1):1–8. https://doi.org/10.1186/s13028-018-0428-y
Nouvel LX, Hygonenq MC, Catays G, Martinelli E, Le Page P, Collin É, Inokuma H, Schelcher F, Citti C, Maillard R (2019) First detection of Mycoplasma wenyonii in France: Identification, evaluation of the clinical impact and development of a new specific detection assay. Comp Immunol Microbiol Infect Dis 63:148–153. https://doi.org/10.1016/j.cimid.2019.01.010
Ritzmann M, Grimm J, Heinritzi K, Hoelzle K, Hoelzle LE (2009) Prevalence of Mycoplasma suis in slaughter pigs, with correlation of PCR results to hematological findings. Vet Microbiol 133(1–2):84–91. https://doi.org/10.1016/j.vetmic.2008.06.015
Sajid MS, Iqbal Z, Khan MN, Muhammad G, Khan MK (2009) Prevalence and associated risk factors for bovine tick infestation in two districts of lower Punjab. Pakistan Prev Vet Med 92(4):386–391. https://doi.org/10.1016/j.prevetmed.2009.09.001
Saki CE, Ozer E (2009) Clinical Eperythrozoon wenyoni (Adler and Ellenbogen, 1934) and Haemobartonella bovis (Donatin and Lestoquard, 1934) infection in a cattle. Fırat Üniv Sağ Bil Vet Derg 23(2):117–118
Santos NJ, Brito DR, Abate HL, Paixão SF, Soares ED, Vieira TS, Garcia JL, Vieira RF, Vidotto O (2018) Hemotropic mycoplasmas infection in water buffaloes (Bubalus bubalis) from northeastern Brazil. Comp Immunol Microbiol Infect Dis 56:27–29. https://doi.org/10.1016/j.cimid.2017.12.003
Sasaoka F, Suzuki J, Hirata TI, Ichijo T, Furuhama K, Harasawa R, Satoh H (2015) Vertical transmission of Mycoplasma wenyonii in cattle, supported by analysis of the ribonuclease P RNA gene. Acta Vet Hung 63(3):271–274. https://doi.org/10.1556/004.2015.025
Shi H, Duan L, Liu F, Hu Y, Shi Z, Chen X, Yang H, Yan B, Yao L (2019) Rhipicephalus (Boophilus) microplus ticks as reservoir and vector of ‘Candidatus Mycoplasma haemobos’ in China. Vet Parasitol 274:108929. https://doi.org/10.1016/j.vetpar.2019.108929
Song Q, Wang L, Fang R, Khan MK, Zhou Y, Zhao J (2013) Detection of Mycoplasma wenyonii in cattle and transmission vectors by the loop-mediated isothermal amplification (LAMP) assay. Trop Anim Health Prod 45(1):247–250. https://doi.org/10.1007/s11250-012-0197-y
Tagawa M, Matsumoto K, Inokuma H (2008) Molecular detection of Mycoplasma wenyonii and ‘Candidatus Mycoplasma haemobos’ in cattle in Hokkaido. Japan Vet Microbiol 132(1–2):177–180. https://doi.org/10.1016/j.vetmic.2008.05.006
Tagawa M, Yamakawa K, Aoki T, Matsumoto K, Ishii M, Inokuma H (2013) Effect of chronic hemoplasma infection on cattle productivity. J Vet Med Sci 13–0119. https://doi.org/10.1292/jvms.13-0119
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Tatsukawa F, Nohara R, Taniguchi T, Goto A, Misawa N, Katamoto H (2020) Detection of Mycoplasma wenyonii and “Candidatus Mycoplasma haemobos” from Japanese Black breeding cows in Kyushu and Okinawa region, southern part of Japan. J Vet Med Sci 20–0505. https://doi.org/10.1292/jvms.20-0505
Ybañez AP, Ybañez RHD, Armonia RKM, Chico JKE, Ferraren KJV, Tapdasan EP, Salces CB, Maurillo BCA, Galon EMS, Macalanda AMC, Moumouni PFA, Xuan X (2019) First molecular detection of Mycoplasma wenyonii and the ectoparasite biodiversity in dairy water buffalo and cattle in Bohol, Philippines. Parasitol Int 70:77–81. https://doi.org/10.1016/j.parint.2019.02.004
Ybañez AP, Ybañez, RHD, Tagawa M (2015) Molecular detection of hemoplasma species (Mycoplasma spp.) in Cattle in Cebu, Philippines. J Adv Vet Res 5(1): 43–46
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T (2012) Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. https://doi.org/10.1186/1471-2105-13-134
Acknowledgements
The authors would like to thank all veterinarians and technicians for their kind help during sample collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
All procedures performed in studies involving animals were in accordance with the ethical standards approved by the Sivas Cumhuriyet University Animal Experiments Local Ethics Committee (Approval number: 65202830–050.04.04–573).
Consent to participate
The consent of all animal owners was sorted before this study was carried out.
Consent for publication
All authors have seen and approved the final version of the manuscript being submitted. They warrant that the article is the authors’ original work, has not received prior publication, and is not under consideration for publication elsewhere.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Erol, U., Sahin, O.F. & Altay, K. Molecular prevalence of bovine hemoplasmosis in Turkey with first detection of Mycoplasma wenyonii and Candidatus Mycoplasma haemobos in cattle and water buffalo. Vet Res Commun 47, 207–215 (2023). https://doi.org/10.1007/s11259-022-09943-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-022-09943-2