The “Nucleotide-binding domain and Leucine-rich Repeat” (NLR) genes are a family of intracellular pattern recognition receptors (PRR) that are a critical component of the metazoan innate immune system, involved in both defense against pathogenic microorganisms and in beneficial interactions with symbionts. To investigate the origin and evolution of the NLR gene family, we characterized the full NACHT domain-containing gene complement in the genome of the sponge, Amphimedon queenslandica. As sister group to all animals, sponges are ideally placed to inform our understanding of the early evolution of this ancient PRR family. Amphimedon queenslandica has a large NACHT domain-containing gene complement that is dominated by bona fide NLRs (n = 135) with varied phylogenetic histories. Approximately half of these have a tripartite architecture that includes an N-terminal CARD or DEATH domain. The multiplicity of the A. queenslandica NLR genes and the high variability across the N- and C-terminal domains are consistent with involvement in immunity. We also provide new insight into the evolution of NLRs in invertebrates through comparative genomic analysis of multiple metazoan and nonmetazoan taxa. Specifically, we demonstrate that the NLR gene family appears to be a metazoan innovation, characterized by two major gene lineages that may have originated with the last common eumetazoan ancestor. Subsequent lineage-specific gene duplication, gene loss and domain shuffling all have played an important role in the highly dynamic evolutionary history of invertebrate NLRs.
Vertical transmission of bacterial symbionts, which is known in many species of sponge (Porifera), is expected to promote strong fidelity between the partners. Combining 16S rRNA gene amplicon sequencing and electron microscopy, we have assayed the relative abundance of vertically-inherited bacterial symbionts in several stages of the life cycle of Amphimedon queenslandica, a tropical coral reef sponge. We reveal that adult A. queenslandica house a low diversity microbiome dominated by just three proteobacterial OTUs, with a single gammaprotebacterium clearly dominant through much of the life cycle. This ontogenetic perspective has revealed that, although vertical transmission occurs very early in development, the inherited symbionts do not maintain proportional dominance of the bacterial community at every developmental stage. A reproductive bottleneck in the A. queenslandica life cycle is larval settlement, when a free-swimming pelagic larva settles out of the water column onto the benthos and completes metamorphoses into the sessile body plan within just 3-4 days. During this dramatic life cycle transition, an influx of environmentally-derived bacteria leads to a major reorganization of the microbiome, potentially challenging the fidelity and persistence of the vertically-inherited symbiotic relationships. However, dominance of the primary, vertically-inherited symbionts is restored in adult sponges. The mechanisms underlying ontogenetic changes in the bacterial community are unknown, including how the dominance of the primary symbionts is restored in the adult sponge-does the host or symbiont regulate this process? Using high-resolution transcriptional profiling in multiple stages of the A. queenslandica life cycle combined with this natural perturbation of the microbiome immediately following larval settlement, we are beginning to identify candidate host genes associated with animal-bacterial crosstalk. Among the sponge host genes upregulated during the times of active microbiome assembly, there is an enrichment of genes potentially involved in innate immunity, including scavenger receptors, and of genes containing eukaryote-like domains, which have elsewhere Fieth et al.Sponge Microbiome Changes through Lifecycle been implicated in host-symbiont interactions. Intriguingly, we also see an enrichment of sponge genes arising from ancient horizontal transfer events from bacteria, which raises the possibility that host-bacterial associations in the evolutionary past may help to regulate host-bacterial associations in the ecological present.
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