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Many gene families are shared across the tree of life between distantly related species because of horizontal gene transfers (HGTs). However, the frequency of HGTs varies strongly between gene families and biotic realms suggesting differential selection pressures and functional bias. One gene family with a wide distribution are FIC-domain containing enzymes (FicDs). FicDs catalyze AMPylation, a post-translational protein modification consisting in the addition of adenosine monophosphate to accessible residues of target proteins. Beside the well-known conservation of FicDs in deuterostomes, we report the presence of a conserved FicD gene ortholog in a large number of protostomes and microbial eukaryotes. We also reported additional FicD gene copies in the genomes of some rotifers, parasitic worms and bivalves. A few dsDNA viruses of these invertebrates, including White spot syndrome virus, Cherax quadricarinatus iridovirus, Ostreid herpesvirus-1 and the beetle nudivirus, carry copies of FicDs, with phylogenetic analysis suggesting a common origin of these FicD copies and the duplicated FicDs of their invertebrate hosts. HGTs and gene duplications possibly mediated by endogenous viruses or genetic mobile elements seem to have contributed to the transfer of AMPylation ability from bacteria and eukaryotes to pathogenic viruses, where this pathway could have been hijacked to promote viral infection.

Supplementary data for the article https://doi.org/10.1098/rstb.2020.0165

Ostreid herpesvirus-1 (OsHV-1) RNAs are enzymatically modified by A-to-I conversions during the infection of Crassostrea gigas. The increase of ADAR1 expression and hyper-editing activity parallel to OsHV-1 RNAs suggests a functional connection between dsRNA editing and antiviral responses. We analyzed 87 RNA-seq data sets from immuno-primed, resistant, and susceptible oysters exposed to OsHV-1 to compare the ADAR hyper-editing levels on host and viral transcripts and trace hyper-editing on the oyster genes. Host RNAs were more hyper-edited than viral RNAs, despite the increased editing of viral RNAs in late infection phases. A set of genes, representing ∼0.5% of the oyster transcriptome and including several tripartite motif-containing sequences, were constantly hyper-edited. Conversely, we identified genes involved in antiviral response, miRNA maturation, and epigenetic regulation that were hyper-edited in specific conditions only. Despite technical and biological bottlenecks that hamper the understanding of the bivalve “RNA editome,” available tools and technologies can be adapted to bivalve mollusks. IMPORTANCE Ostreid herpesvirus-1 (OsHV-1) is a harmful pathogen of bivalve species, such as oysters. However, knowledge is lacking about host–virus interactions at the molecular level, hampering the possibility of a correct management of viral outbreaks and related massive mortalities. Notably, OsHV-1 transcripts are massively modified by host RNA editing enzyme during infection, resulting in multiple A-to-I variations along RNAs assuming double-strand conformations. The impact of these modifications on host transcripts is, however, not completely clear. Analyzing RNA-seq data of oysters infected with OsHV-1, we revealed that ∼0.5% of the oyster transcriptome is always enzymatically modified by ADAR, whereas genes involved in antiviral response, miRNA maturation, and epigenetic regulation were hyper-edited in specific conditions only. Despite our results, relevant t

The interleukin-17 (IL-17) family consists of proinflammatory cytokines conserved during evolution. A comparative genomics approach was applied to examine IL-17 throughout evolution from poriferans to higher vertebrates. Cnidaria was highlighted as the most ancient diverged phylum, and several evolutionary patterns were revealed. Large expansions of the IL-17 repertoire were observed in marine molluscs and echinoderm species. We further studied this expansion in filter-fed Mytilus galloprovincialis, which is a bivalve with a highly effective innate immune system supported by a variable pangenome. We recovered 379 unique IL-17 sequences and 96 receptors from individual genomes that were classified into 23 and 6 isoforms after phylogenetic analyses. Mussel IL-17 isoforms were conserved among individuals and shared between closely related Mytilidae species. Certain isoforms were specifically implicated in the response to a waterborne infection with Vibrio splendidus in mussel gills. The involvement of IL-17 in mucosal immune responses could be conserved in higher vertebrates from these ancestral lineages

Bivalves are a diverse mollusc group of economic and ecological importance. An evident resilience to pollution, parasites and extreme environments makes some bivalve species important models for studying adaptation and immunity. Despite substantial progress in sequencing projects of bivalves, information on non-coding genes and gene-regulatory aspects is still lacking. Here, we review the current repertoire of bivalve microRNAs (miRNAs), important regulators of gene expression in Metazoa. We exploited available short non-coding RNA (sncRNA) data for Pinctada martensii, Crassostrea gigas, Corbicula fluminea, Tegillarca granosa and Ruditapes philippinarum, and we produced new sncRNA data for two additional bivalves, the Mediterranean mussel Mytilus galloprovincialis and the blood clam Scapharca broughtonii. We found substantial heterogeneity and incorrect annotations of miRNAs; hence, we reannotated conserved miRNA families using recently established criteria for bona fide microRNA annotation. We found 106 miRNA families missing in the previously published bivalve datasets and 89 and 87 miRNA complements were identified in the two additional species. The overall results provide a homogeneous and evolutionarily consistent picture of miRNAs in bivalves and enable future comparative studies. The identification of two bivalve-specific miRNA families sheds further light on the complexity of transcription and its regulation in bivalve molluscs