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Background   Theileria orientalis  is a tick-borne hemoparasite that causes anemia, ill thrift, and death in cattle globally. The Ikeda strain of  T.   orientalis  is more virulent than other strains, leading to severe clinical signs and death of up to 5% of affected animals. Within the Asia–Pacific region, where it affects 25% of Australian cattle,  T.   orientalis  Ikeda has a significant economic impact on the cattle industry. In 2017,  T.   orientalis  Ikeda was detected in a cattle herd in Albermarle County, Virginia, United States. Months earlier, the U.S. was alerted to the invasion of the Asian longhorned tick,  Haemaphysalis longicornis,  throughout the eastern U.S. Abundant  H.   longicornis  ticks were identified on cattle in the  T.   orientalis- affected herd in VA, and a subset of ticks from the environment were PCR-positive for  T.   orientalis  Ikeda. A strain of  T.   orientalis  from a previous U.S. outbreak was not transmissible by  H.   longicornis ; however,  H.   longicornis  is the primary tick vector of  T.   orientalis  Ikeda in other regions of the world. Thus, the objective of this study was to determine whether invasive  H.   longicornis  ticks in the U.S. are competent vectors of  T.   orientalis  Ikeda.    Methods  Nymphal  H.   longicornis  ticks were fed on a splenectomized calf infected with the VA-U.S.- T.   orientalis  Ikeda strain. After molting, a subset of adult ticks from this cohort were dissected, and salivary glands assayed for  T.   orientalis  Ikeda via qPCR. The remaining adult ticks from the group were allowed to feed on three calves. Calves were subsequently monitored for  T.   orientalis  Ikeda infection via blood smear cytology and PCR.    Results  After acquisition feeding on a VA-U.S.- T.   orientalis  Ikeda-infected calf as nymphs, a subset of molted adult tick salivary glands tested positive by qPCR for  T.   orientalis  Ikeda. Adult ticks from the same cohort successfully transmitted  T.   orientalis  Ikeda to 3/3 naïve calves, each of which developed parasitemia reaching 0.4–0.9%.    Conclusions  Our findings demonstrate that U.S.  H.   longicornis  ticks are competent vectors of the VA-U.S.- T.   orientalis  Ikeda strain. This data provides important information for the U.S. cattle industry regarding the potential spread of this parasite and the necessity of enhanced surveillance and control measures.Supplementary Information  The online version contains supplementary material available at 10.1186/s13071-021-04659-9.

A U.S. isolate of Theileria orientalis, Ikeda genotype, is transmitted to cattle by the invasive Asian longhorned tick, Haemaphysalis longicornis