Genome assembly and annotation of Periplaneta americana reveal a comprehensive cockroach allergen profile

Background One of the most common cockroach types in urban areas, the American cockroach (Periplaneta americana), has been reported to impose an increased risk of allergies and asthma. Limited groups of allergens (Per a 1–13) have been identified in this species due to the lack of genome‐related information. Methods To expand the allergen profile of P. americana, genomic, transcriptomic, and proteomic approaches were applied. With the support of a high‐quality genome assembled using nanopore, Illumina, and Hi‐C sequencing techniques, potential allergens were identified based on protein homology. Then, using enzyme‐linked immunosorbent assay, selected allergens were tested in Thai patients allergic to P. americana. Results A chromosomal‐level genome of P. americana (3.06 Gb) has been assembled with 94.6% BUSCO completeness, and its contiguity has been significantly improved (N50 = 151 Mb). A comprehensive allergen profile has been characterized, with seven novel groups of allergens, including enolase (Per a 14), cytochrome C (Per a 15), cofilin (Per a 16), alpha‐tubulin (Per a 17), cyclophilin (Per a 18), porin3 (Per a 19), and peroxiredoxin‐6 (Per a 20), showing IgE sensitivity in enzyme‐linked immunosorbent assay. A new isoallergen of tropomyosin (Per a 7.02) and multiple potential isoallergens of Per a 5 were revealed using bioinformatics and proteomic approaches. Additionally, comparative analysis of P. americana with the closely related Blattodea species revealed the possibility of cross‐reaction. Conclusion The high‐quality genome and proteome of P. americana are beneficial in studying cockroach allergens at the molecular level. Seven novel allergen groups and one isoallergen in Per a 7 were identified. Our high‐quality genome (3.06 Gb) and precisely annotated proteome (29,939) of the American cockroach help revealed a broader allergen spectrum. Seven novel allergen groups Per a 14 to Per a 20 and one isoallergens (Per a 7.02) were validated using ELISA in Thai cohort. Comparative analysis of P. americana with the closely related Blattodea species revealed the possibility of cross‐reaction.Abbreviations: ELISA, enzyme‐linked immunosorbent assay; gDNA, genomic DNA; GST, glutathione S‐transferases; SPT, skin prick test; MS, mass spectrometry