The Unique Antimicrobial Recognition and Signaling Pathways in Tardigrades with a Comparison Across Ecdysozoa.

Abstract

Tardigrades are microscopic animals known to withstand unfavorable abiotic conditions. These animals are also constantly exposed to biotic stresses, including parasites and internal microbiomes. However, the tardigrade immune mechanisms against these biotic stresses are largely uncharacterized. Due to the contentious phylogenetic position of tardigrades, it is not intuitive whether they possess an immune system more similar to that of arthropods (, Toll, Imd, and JNK pathways of the antimicrobial response) or to that of nematodes (, the Tir-1/Nsy-1/Sek-1/Pmk-1/Atf-7 signaling cassette [called Tir-1 pathway here]) in ). In this study, comparative genomic analyses were conducted to mine homologs of canonical and immune pathway genes from eight tardigrades ( cf. , , , , , , cf. , and ) and four non-arthropod ecdysozoans (two onychophorans: sp. and ; one nematomorph: ; and one priapulan: ) in order to provide insights into the tardigrade antimicrobial system. No homologs of the intracellular components of the Toll pathway were detected in any of the tardigrades examined. Likewise, no homologs of most of the Imd pathway genes were detected in any of the tardigrades or any of the other non-arthropod ecdysozoans. Both the JNK and Tir-1 pathways, on the other hand, were found to be conserved across ecdysozoans. Interestingly, tardigrades had no detectable homologs of , the major activator of antimicrobial response gene expression. Instead, tardigrades appear to possess distantly related homologs. Overall, our results show that tardigrades have a unique gene pathway repertoire that differs from that of other ecdysozoans. Our study also provides a framework for future studies on tardigrade immune responses.