Comparative genomic study of arachnid immune systems indicates loss of beta‐1,3‐glucanase‐related proteins and the immune deficiency pathway

Abstract

Analyses of arthropod genomes have shown that the genes in the different innate humoral immune responses are conserved. These genes encode proteins that are involved in immune signalling pathways that recognize pathogens and activate immune responses. These immune responses include phagocytosis, encapsulation of the pathogen, and production of effector molecules for pathogen elimination. So far, most studies have focused on insects leaving other major arthropod groups largely unexplored. Here we annotate the immune related genes of six arachnid genomes and present evidence for a conserved pattern of some immune genes, but also evolutionary changes in the arachnid immune system. Specifically, our results suggest that the family of recognition molecules of Beta-1,3-glucanase-related proteins (βGRPs) and the genes from the immune deficiency (IMD) signalling pathway have been lost in a common ancestor of arachnids. These findings are consistent with previous work suggesting that the humoral immune effector proteins are constitutively produced in arachnids in contrast to insects, where these have to be induced. Further functional studies are needed to verify this. We further show that the full hemolymph clotting cascade found in the horseshoe crab is retrieved in most arachnid genomes. Tetranychus lacks at least one major component, although it is possible that this cascade could still function through recruitment of a different protein. The gel-forming protein in horseshoe crabs, coagulogen, was not recovered in any of the arachnid genomes, however, it is possible that the arachnid clot consists of a related protein, spätzle, that is present in all of the genomes.

Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin

“…Upon replacing either the asparagine or glutamine residues with different amino acids only catecholoxidase activity is possible [161]. In the absence of a true PO, chelicerates rely on the inducible PO activity of Hc as a substitute [28, 30, 162, 163, 203, 204]. Lately, Hc was found to be a major component of clots formed during hemostasis in the spider, Acanthoscurria geniculata .…”

p47 licenses activation of the immune deficiency pathway in the tick Ixodes scapularis

“…Notably, homologs of many upstream IMD pathway genes were absent. For instance, transmembrane PGRPs, the central adaptor Imd, and FADD were undetectable through bioinformatics analysis (43)(44)(45)(46)(47). Nonetheless, a functional IMD circuit was discovered in I. scapularis (38), underlining the unexplored diversity in arthropod immunity that may be leveraged to develop strategies to prevent vector-borne diseases (41,43,48).…”

Evidence of an Antimicrobial Peptide Signature Encrypted in HECT E3 Ubiquitin Ligases

“…Identification of many classes of antimicrobial peptides that appeared early in evolution (17–21), such as glycine-rich peptides (19, 32, 33), tachyplesin-like HDPs (19, 34), defensins (19–21), lysozymes (20), and hemocyanin-derived antifungal peptides (19, 35) are consistent with their phylogenetic position at the base of extant arthropods’ phylogeny (19, 20, 34–36). Thus, investigating the arachnid innate immune peptidome is a promising approach to identify ancient host defense effectors, including cryptic HDPs.…”

“…C-type lysozymes, classical players of innate immunity, are ubiquitous and constitutively expressed in leukocytes, providing an immediate defensive barrier to invading pathogens (20, 41, 58). Because context-specific co-expression of lysozymes with other host defense elements such as HDPs suggests synergy between these factors (41, 59), we investigated whether oligoventin has a mutually potentiating effect on the G. gallus C-lysozyme, as C-type lysozymes from arachnids are highly similar to avian lysozymes (Figure 1D).…”