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.

Pest management of postharvest potatoes: lethal, sublethal and transgenerational effects of the ectoparasitic mite Pyemotes zhonghuajia on the potato worm Phthorimaea operculella

“…In ectophagous idiobiont parasitoids, reproductive females inject venom that permanently paralyzes the hosts and rapidly suppresses their immune responses 29,31,47–54 . Suppression of host immune responses by parasitoids may impose host physiology changes which alter host immature development and affect adult longevity and fecundity 47,52,55–59 .…”

“…In ectophagous idiobiont parasitoids, reproductive females inject venom that permanently paralyzes the hosts and rapidly suppresses their immune responses. 29,31,[47][48][49][50][51][52][53][54] Suppression of host immune responses by parasitoids may impose host physiology changes which alter host immature development and affect adult longevity and fecundity. 47,52,[55][56][57][58][59] In this study, we demonstrated that P. zhonghuajia parasitism has lethal, sublethal and transgenerational effects on the PTM.…”

“…Pyemotes zhonghuajia Yu, Zhang & He (Prostigmata: Pyemotidae) is a generalist ectoparasitic idiobiont mite, in which the adult females parasitize and prey on different immature stages of insect species in Coleoptera, Lepidoptera, Hymenoptera, Homoptera and Isoptera. [21][22][23][24][25][26][27][28][29][30][31] The females thus have the life-history traits of both parasitioids and predators. P. zhonghuajia is a viviparous species, i.e., the immature offspring develop in the mother's opisthosoma.…”

“…Prior to feeding and breeding their offspring on the hosts, the females paralyze the hosts by injecting venomous saliva 31,36,37 and a single mite can paralyze a host (i.e., insect larva) of 166 000 37 or even 680 000 times its own weight 31 . Venom compounds including neurotoxin, dermonecrotic toxin and agatoxin gene families that are associated with toxicity have been identified in P. zhonghuajia 29 . Due to their short lifecycle, high fecundity and strong toxicity to hosts, Pyemotes mites have long been considered as potential biocontrol agents, mass‐produced and released to control insect pests in fields 21–24,28–33,38–44 .…”

“…31 Venom compounds including neurotoxin, dermonecrotic toxin and agatoxin gene families that are associated with toxicity have been identified in P. zhonghuajia. 29 Due to their short lifecycle, high fecundity and strong toxicity to hosts, Pyemotes mites have long been considered as potential biocontrol agents, mass-produced and released to control insect pests in fields. [21][22][23][24][28][29][30][31][32][33][38][39][40][41][42][43][44] To our knowledge, only a few researchers 38,45,46 have attempted to control insect pests of storage products using Pyemotes mites, and their biological control efficiency, especially on the PTM in storages, is largely unknown.…”