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Abstract
The innate immune system helps animals to navigate the microbial world. The response to microbes relies on the specific recognition of microbial-associated molecular patterns (MAMPs) by immune receptors. Sponges (phylum Porifera), as early-diverging animals, provide insights into conserved mechanisms for animal-microbe crosstalk. However, experimental data is limited. We adopted an experimental approach followed by RNA-Seq and differential gene expression analysis in order to characterise the sponge immune response. Two Mediterranean species, Aplysina aerophoba and Dysidea avara, were exposed to a “cocktail” of MAMPs (lipopolysaccharide and peptidoglycan) or to sterile artificial seawater (control) and sampled 1 h, 3 h, and 5 h post-treatment for RNA-Seq. The response involved, first and foremost, a higher number of differentially-expressed genes in A. aerophoba than D. avara. Secondly, while both species constitutively express a diverse repertoire of immune receptors, they differed in their expression profiles upon MAMP challenge. The response in D. avara was mediated by increased expression of two NLR genes, whereas the response in A. aerophoba involved SRCR and GPCR genes. From the set of annotated genes we infer that both species activated apoptosis in response to MAMPs while in A. aerophoba phagocytosis was additionally stimulated. Our study assessed for the first time the transcriptomic responses of sponges to MAMPs and revealed conserved and species-specific features of poriferan immunity as well as genes potentially relevant to animal-microbe interactions.
Highlights
The advent of microbial life on earth predates that of animals by at least 3 billion years[1]
They originated from a total of 18 samples from A. aerophoba and 17 samples from D. avara, corresponding to three biological replicates per treatment within each of the three time points
The sponges responded by increased expression of a subset of relevant receptors (i.e., nucleotide-binding domain and leucine-rich repeat containing receptors (NLRs) in D. avara, scavenger receptor cysteine-rich (SRCR) and G-protein coupled receptors (GPCRs) in A. aerophoba) and the transduction of signals by kinase cascades that likely yield apoptosis and regulation of metabolic processes
Summary
The advent of microbial life on earth predates that of animals by at least 3 billion years[1]. NLR-mediated activation of the mitogen-activated protein kinase (MAPK) signalling cascade (e.g., p38, JNKs) and caspases results in reactive oxygen species formation, inflammatory processes, production of antimicrobial peptides, as well as cell death[22,23] Other receptor families, such as the scavenger receptor cysteine-rich (SRCR) and lectins, add to the diverse repertoire of immune receptors found in most animals[10]. Sponges (phylum Porifera) are among the earliest-diverging multicellular animals and considered key to understanding the origins of animal processes, including animal-microbe interactions[26,27] Due to their sessile filter-feeder lifestyle, sponges constantly encounter microbes from the seawater, which serve as a food source, but at the same time maintain stable species-specific symbiotic communities[28]. Empirical evidence of such functions remains scarce[37,38,39]
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