Genome of the invasive North American Haemaphysalis longicornis tick as a template for bovine anti-tick vaccine discovery.

Abstract

Background: The ixodid tick Haemaphysalis longicornis Neumann, commonly referred to as the Asian longhorned tick, has expanded its range outside of East Asia into countries such as Australia, New Zealand, and the United States. Since the first U.S. detection in 2017, H. longicornis has spread to 21 states and the District of Columbia and has been implicated as a vector of various human and animal pathogens including Theileria orientalis Ikeda genotype, a causal agent of bovine theileriosis. Facilitated in part by the parthenogenetic nature of invasive populations, this tick has become a paramount threat to agricultural rangelands and U.S. livestock production. Reliance on traditional acaricides for vector control selects for resistant individuals, reducing the effectiveness of many chemical tools over time. Thus, focus has shifted to alternative control mechanisms including anti-tick vaccine development. To further such research, here we sequence and assemble a high-quality H. longicornis genome and robust gene catalog from invasive North American ticks while also providing an organ-specific transcriptomic expression catalog and in-depth informatic screening of the tick proteome for potential bovine antigenic molecules with potential utility as vaccine candidates.

Results: Using a combination of PacBio HiFi single-molecule sequencing and Hi-C chromosome conformation capture data, our genome assembly contains 270 scaffolds and spans a haploid genome size of 3.09 Gbp with an N50 of 213.4 Mbp. Gene prediction identified 21,947 high-confidence gene structures containing 96.2% of the core Arthropoda odb10 orthologs. Our organ-specific transcriptome library comprising salivary glands, midgut, ovaries, foreleg and hindleg additionally highlights potential anti-tick vaccine candidates and metabolic pathways to target for future in vitro trials.

Conclusions: Single-molecule sequencing of a triploid, parthenogenetic North American Haemaphysalis longicornis tick allowed for the generation of a highly contiguous genome assembly that, when coupled with extensive transcriptome profiling, resulted in a robust gene catalog containing multiple candidates for further study as anti-tick vaccine antigens.