A Long-Read Genome Assembly of a Native Mite in China Pyemotes zhonghuajia Yu, Zhang & He (Prostigmata: Pyemotidae) Reveals Gene Expansion in Toxin-Related Gene Families

Abstract

Pyemotes zhonghuajia Yu, Zhang & He (Prostigmata: Pyemotidae), discovered in China, has been demonstrated as a high-efficient natural enemy in controlling many agricultural and forestry pests. This mite injects toxins into the host (eggs, larvae, pupae, and adults), resulting in its paralyzation and then gets nourishment for reproductive development. These toxins have been approved to be mammal-safe, which have the potential to be used as biocontrol pesticides. Toxin proteins have been identified from many insects, especially those from the orders Scorpions and Araneae, some of which are now widely used as efficient biocontrol pesticides. However, toxin proteins in mites are not yet understood. In this study, we assembled the genome of P. zhonghuajia using PacBio technology and then identified toxin-related genes that are likely to be responsible for the paralytic process of P. zhonghuajia. The genome assembly has a size of 71.943 Mb, including 20 contigs with a N50 length of 21.248 Mb and a BUSCO completeness ratio of 90.6% (n = 1367). These contigs were subsequently assigned to three chromosomes. There were 11,183 protein coding genes annotated, which were assessed with 91.2% BUSCO completeness (n = 1066). Neurotoxin and dermonecrotic toxin gene families were significantly expanded within the genus of Pyemotes and they also formed several gene clusters on the chromosomes. Most of the genes from these two families and all of the three agatoxin genes were shown with higher expression in the one-day-old mites compared to the seven-day-pregnant mites, supporting that the one-day-old mites cause paralyzation and even death of the host. The identification of these toxin proteins may provide insights into how to improve the parasitism efficiency of this mite, and the purification of these proteins may be used to develop new biological pesticides.

Keywords: Pyemotes; genome annotation; protein; toxin.

Figure 1

Histogram shows the number of genes assigned to different groups. The “1:1:1” and “N:N:N” groups represent single- and multi-copy genes found in all the species. The group “Acariformes” represents orthologs unique to Acariformes. The “Others” group indicates other orthologs which do not belong to any above-mentioned ortholog categories. The group “Unassigned” represent the orthologs which can’t be assigned to any orthogroups.

Figure 2

Dating tree with node values representing the number of expanded, contracted.

Figure 3

Top fifteen significantly expanded families with gene numbers of the families shown above the bars.

Figure 4

Distribution of toxin genes on the chromosomes and phylogenetic trees of the three toxin gene classes. (A) Distribution of toxin genes on the chromosomes. Blue: neurotoxin genes; Orange: agatoxin genes; Purple: dermonecrotic toxin genes. (B–D) Phylogenetic trees of neurotoxin genes, dermonecrotic toxin genes, and agatoxin genes. The “*” indicates the gene was shown with higher expression in the seven-day-pregnant mites compared with the one-day-old mites. The accession numbers of all the sequences used in the phylogenies are listed in Supplementary Table S12.

Figure 4

Distribution of toxin genes on the chromosomes and phylogenetic trees of the three toxin gene classes. (A) Distribution of toxin genes on the chromosomes. Blue: neurotoxin genes; Orange: agatoxin genes; Purple: dermonecrotic toxin genes. (B–D) Phylogenetic trees of neurotoxin genes, dermonecrotic toxin genes, and agatoxin genes. The “*” indicates the gene was shown with higher expression in the seven-day-pregnant mites compared with the one-day-old mites. The accession numbers of all the sequences used in the phylogenies are listed in Supplementary Table S12.

Figure 4

Distribution of toxin genes on the chromosomes and phylogenetic trees of the three toxin gene classes. (A) Distribution of toxin genes on the chromosomes. Blue: neurotoxin genes; Orange: agatoxin genes; Purple: dermonecrotic toxin genes. (B–D) Phylogenetic trees of neurotoxin genes, dermonecrotic toxin genes, and agatoxin genes. The “*” indicates the gene was shown with higher expression in the seven-day-pregnant mites compared with the one-day-old mites. The accession numbers of all the sequences used in the phylogenies are listed in Supplementary Table S12.

Figure 4

Distribution of toxin genes on the chromosomes and phylogenetic trees of the three toxin gene classes. (A) Distribution of toxin genes on the chromosomes. Blue: neurotoxin genes; Orange: agatoxin genes; Purple: dermonecrotic toxin genes. (B–D) Phylogenetic trees of neurotoxin genes, dermonecrotic toxin genes, and agatoxin genes. The “*” indicates the gene was shown with higher expression in the seven-day-pregnant mites compared with the one-day-old mites. The accession numbers of all the sequences used in the phylogenies are listed in Supplementary Table S12.