Improved genome assembly provides new insights into the environmental adaptation of the American cockroach, Periplaneta americana

Abstract

The synanthropic pest and a model organism for entomological research, American cockroach, Periplaneta americana (Linnaeus), can survive in unfavorable environments for humans. To investigate the genetic mechanisms of success in environmental adaptation of P. americana, we de novo reassembled its whole genome based on next-generation sequencing and PacBio sequencing. The final genome reassembly consisted of approximately 3.34 Gb with scaffold N50 of 465.51 Kb. The completeness (95.4%) of the complete genome was evaluated with single-copy orthologous genes using BUSCO. We identified 18,618 protein-coding genes, 16,443 (88.32%) of which were well supported by public protein databases. We identified 482.04 Mb (approximately 14.45%) repeat elements, 1,385,093 perfect microsatellites simple sequence repeats in P. americana genome, which was higher than other four Blattaria insects. Comparative genomics analysis revealed obvious expansion in the gene families associated with chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), which provided the necessary information for functional characterization of the chemosensory receptors of P. americana, with potential for new or refined applications of semiochemicals-based control of this pest insect. Similarly, gene families (cytochrome P450s, carboxyl/choline esterases, and UDP-glycosyl-transferases) encoding receptors for bitter or toxic substances and detoxification enzymes were obviously expanded in P. americana, enabling its ability to detect and detoxify many toxins. Enrichment analysis of positively selected genes in P. americana revealed items associated with metabolic process and catalytic activity, which possibly contributed to the pesticide resistance of P. americana. We also analyzed the homologs to antimicrobial peptide genes reported in the Drosophila genome, and identified two attacins and seven defensins in P. americana. Our data and findings will substantially facilitate molecular studies in P. americana, including elucidation of detoxification mechanisms of xenobiotic, as well as development of new pest management strategies for the control of pests like P. americana.

Keywords: Periplaneta americana; comparative genomics; environmental adaptation; gene family expansion; positive selection.