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Saliva and silk proteins in spider mites: dual roles in feeding and silk fiber coating

ABSTRACT: Spider mites are leaf cell-sucking herbivores that spin nanoscale silk fibers released from their second mouthpart appendages. Previous studies computationally predicted 17 silk protein genes by whole genome sequencing in the two-spotted spider mite, Tetranychus urticae, while two novel candidates, Fibroin-1 and Fibroin-2, were detected in the silk proteome. In addition, Fibroin-1, sFibroin-1 (high sequence similarity to Fibroin-1), and Fibroin-2 proteins were also detected in the saliva proteome. We investigated whether these three proteins function as silk, saliva, or both. The mRNA for Fibroin-1, sFibroin-1, and Fibroin-2 were all expressed in the salivary glands. Micro-CT scanning confirmed no direct connection between salivary glands and silk glands, i.e., saliva and silk meet each other during simultaneous secretion and spinning. Silk proteomics performed in the present study detected proteins encoded by 8 of the 17 originally predicted genes, as well as Fibroin-1, sFibroin-1, and Fibroin-2 proteins. In addition, cryo-SEM imaging visualized a bead-on-a-string pattern formed by a fluid on the silk fiber, as well as a fluid patch that remains at the piercing site on the leaf surface after mite feeding. Furthermore, RNAi-mediated silencing of Fibroin-1 and sFibroin-1 reduced the feeding duration of mites, resulting in low survival and fecundity. Fibroin-2 RNAi reduced the thickness of single filaments of silk fibers. These results suggest that Fibroin-1, sFibroin-1, and Fibroin-2 proteins are secreted from the salivary glands and then adhere to silk fibers. Fibroin-1 and sFibroin-1 proteins support mites establishing a stable piercing site by adhering the tip of the mouthparts to the leaf surface to suck leaf cell contents with their stylets, while Fibroin-2 coats silk fibers. Eight originally predicted genes are still candidates for silk protein genes. This study revealed the two roles of saliva in leaf cell-sucking herbivorous mites, which include stabilizing mouthparts during feeding and coating silk fibers, providing them with adhesive properties.

ORGANISM(S): Cellular Organisms

SUBMITTER: Takeshi Suzuki

PROVIDER: PXD059809 | JPOST Repository | Wed Aug 27 00:00:00 BST 2025

REPOSITORIES: jPOST

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			Action	DRS
	230607_Proteome_Tu_RNAi_Fib1_1.raw	Raw
	230607_Proteome_Tu_RNAi_Fib1_2.raw	Raw
	230607_Proteome_Tu_RNAi_Fib2_1.raw	Raw
	230607_Proteome_Tu_RNAi_Fib2_2.raw	Raw
	230607_Proteome_Tu_RNAi_Mix_1.raw	Raw

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Project description:In addressing R. microplus - A. marginale interactions, we propose and test three linked hypotheses. The first is that the tick gene response is organ specific: the midgut gene regulation is unique during feeding and during acquisition of A. marginale as compared to the salivary gland. This distinction is relevant as the two organs serve very different roles in the transmission biology of A. marginale with early survival and replication within the midgut epithelium, composed of highly phagocytic cells, required for initial colonization while a second round of replication in the salivary gland acini, composed of highly secretory cells, is required for transmission of an infectious dose in the saliva. Importantly, both the midgut epithelium and salivary glands have been identified as separate and distinct barriers for transmission of A. marginale and thus represent two potential sites where transmission could be blocked. The second hypothesis to be tested is that the salivary gland transcriptome is temporally dynamic. Initiation of tick attachment and feeding involves secretion of a virtual pharmacopeia including lytic enzymes, anticoagulants, and inhibitors of the mammalian innate immune and nocioceptive systems. Concomitantly, the acini provide an environment where A. marginale replicates >100 fold and are secreted into the saliva. Prior studies show that duration of feeding is a critical component of transmission efficiency, with increased efficiency positively correlated with time of tick feeding. The third hypothesis to be tested is that A. marginale colonization does not significantly modulate the tick midgut and salivary gland transcriptome. This hypothesis is based on observations by ourselves and others that tick infection does not impart a significant fitness cost on the vector. This is in contrast to other bacterial and protozoal pathogens that have dramatic effects on success of tick attachment, engorgement, and survival. A. marginale, similar to other tick-borne pathogens in the Family Anaplasmataceeae, is believed to have evolved from an arthropod-specific bacterium with relatively late adaptation to specific niches in mammalian hosts. Consequently, we predict that A. marginale is well adapted to its tick vector and utilizes the normal signaling pathways of the feeding tick with few, if any, effects on the midgut and salivary gland transcriptome. In this manuscript, we report the testing of these three hypotheses and present the results in context of the vector-pathogen-mammalian host interaction at the time of transmission. A Roche NimbleGen high-density gene expression microarray was custom designed based on the expressed sequence tag (EST) database, B. microplus Gene Index Version 2 (BmiGI V2) for R. microplus. The expression level of 14,447 R. microplus genes was analyzed from total RNA extracted from 10 different tick tissue samples; 30 arrays were included since triplicates of each different sample were analyzed as follow: unfed (midgut and salivary glands), blood feeding (2 days midgut and 2, 6 and 9 days salivary glands), A. marginale-infected blood feeding (2 days midgut and 2, 6 and 9 days salivary glands).

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Saliva and silk proteins in spider mites: dual roles in feeding and silk fiber coating

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