The putative immune recognition repertoire of the model cnidarian Hydractinia symbiolongicarpus is large and diverse

Abstract

Immune recognition of molecular patterns from microorganisms or self-altered cells activate effector responses that neutralize and eliminate these potentially harmful agents. In virtually every metazoan group the process is carried out by pattern recognition receptors, typically constituted by immunoglobulin (Ig), leucine rich repeat (LRR), and/or lectin domains. In order to get insights into the ancestral immune recognition repertoire of animals, we have sequenced the transcriptome of bacterially challenged colonies of the model cnidarian Hydractinia symbiolongicarpus using the Illumina platform. Over 116,000 assembled contigs were annotated by sequence similarity, domain architecture, and functionally. From these, a subset of 315 unique transcripts was predicted as the putative immune recognition repertoire of H. symbiolongicarpus. Interestingly, canonical Toll-like receptors (TLR) were not predicted, nor any transmembrane protein with the Toll/interleukine-1 receptor (TIR) domain. Yet, a variety of predicted proteins with transmembrane domains associated with LRR ectodomains were identified, as well as homologs of the key transduction factor NF-kB, and its associated regulatory proteins. This also has been documented in Hydra, and suggests that recognition and signaling initiation has been decoupled in the TLR system of hydrozoans. In contrast, both canonical and non-canonical NOD-like receptors were identified in H. symbiolongicarpus, showing a higher diversity than the TLR system and perhaps a wider functional landscape. The collection of Ig-like containing putative immune recognition molecules was diverse, and included at least 26 unique membrane-bound predicted proteins and 88 cytoplasmic/secreted predicted molecules. In addition, 25 and 5 transcripts encoding the Ig-like containing allorecognition determinants ALR1 and ALR2, respectively, were identified. Sequence and phylogenetic analyses suggested the presence of various transcriptionally active alr loci, and the action of recombination-based mechanisms diversifying them. Transcripts encoding at least six lectin families with putative roles in immune recognition were found, including 19 unique C-type lectins and 21 unique rhamnose-binding lectins. Other predicted immune recognition receptors included scavenger receptors from three families, lipopolysaccharide-binding proteins, cell-adhesion molecules and thioester-bond containing proteins. This analysis demonstrated that the putative immune recognition repertoire of H. symbiolongicarpus is large and diverse.