Hologenome analysis of two marine sponges with different microbiomes

Abstract

BackgroundSponges (Porifera) harbor distinct microbial consortia within their mesohyl interior. We herein analysed the hologenomes of Stylissa carteri and Xestospongia testudinaria, which notably differ in their microbiome content.ResultsOur analysis revealed that S. carteri has an expanded repertoire of immunological domains, specifically Scavenger Receptor Cysteine-Rich (SRCR)-like domains, compared to X. testudinaria. On the microbial side, metatranscriptome analyses revealed an overrepresentation of potential symbiosis-related domains in X. testudinaria.ConclusionsOur findings provide genomic insights into the molecular mechanisms underlying host-symbiont coevolution and may serve as a roadmap for future hologenome analyses.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2501-0) contains supplementary material, which is available to authorized users.

The Holo-Transcriptome of a Calcified Early Branching Metazoan

“…Taxonomic assignment as performed by MEGAN employs protein-coding genes. Interestingly, in comparison to previously reported sponge transcriptomes (Riesgo et al, 2014;Ryu et al, 2016) the Vaceletia sp. transcriptome contains by far the highest proportion of bacterially derived contigs (40%) in comparison to high microbial abundance (HMA) sponges such as X. testudinaris (1.4%), C. nucula (7.5%), and C. candelabrum (13.7%).…”

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

“…Evidence for the involvement of SRCR domain-containing proteins in immunity in poriferans includes the expression of membrane-associated SRCR proteins on spherule cells that appear to be involved in cell aggregation in Geodia cydonium (Blumbach et al, 1998). Perhaps even more compelling, an SRCR domain-containing protein is highly upregulated when the sponge Petrosia ficiformis is colonized by symbiotic cyanobacteria (Steindler et al, 2007), and the LMA sponge S. carteri very interestingly has an expanded complement of SRCR-like domains compared to the HMA sponge X. testudinaria (Ryu et al, 2016). Notably, the SRCR factors upregulated in A. queenslandica postlarvae are composed of SRCR repeats that show structural similarity to those of vertebrate DMBT1, which binds directly to bacterial proteins and is linked with immune-related NLR and TLR signaling (Rosenstiel et al, 2007).…”

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

“…While these studies have provided insight into the true complexity of the sponge-bacteria association, they also leave many important questions unaddressed, as few studies have applied an experimental approach to dissect the host's role in controlling the composition of its bacterial community (but see Steindler, et al 2007;Ryu, et al 2016). The availability of a nearcomplete sequenced genome (Srivastava, et al 2010), easy access to biological material , and a combination of biological traits make the haplosclerid demosponge…”

“…Indeed, the highly conserved innate immune genes encoded in the A. queenslandica genome, including a complete Toll-like receptor signalling pathway, as well as large complements of both cytosolic and extracellular PRRs, provide the first clues suggesting that the ancient innate immune system may play a significant role in mediating spongebacteria interactions Yuen, et al 2014). The most multifarious of these PRRs include 135 genes encoding bona fide members of the nucleotide-binding domain and leucine-rich containing gene family (NLRs) as well as nearly 300 genes from the scavenger receptor cysteine-rich domain-containing (SRCR) gene family, which are putatively involved in MAMP recognition (Yuen, et al 2014;Ryu, et al 2016). These large complements suggest that this morphologically simple animal without a classical adaptive immune system could have the capacity to detect a large and diverse array of microbial ligands, which perhaps allows it to distinguish and subsequently generate specific responses to foreign and symbiotic bacteria (Degnan 2015).…”

“…These large complements suggest that this morphologically simple animal without a classical adaptive immune system could have the capacity to detect a large and diverse array of microbial ligands, which perhaps allows it to distinguish and subsequently generate specific responses to foreign and symbiotic bacteria (Degnan 2015). Indeed, it has been hypothesised that these large lineage-specific expansions of putative PRRs could have emerged in the sponge as a result of co-evolution with their resident bacteria (Yuen, et al 2014;Ryu, et al 2016). It is thus interesting to note that, in addition to the direct exchange of metabolites, resident bacteria could also affect the metabolism of their animal host through modulation of the innate immune response (Hur and Lee 2015;Boulange, et al 2016).…”