Marine Sponge Holobionts in Health and Disease

Abstract

Sponges—like all multicellular organisms—are holobionts, complex ecosystems comprising the host and its microbiota. The symbiosis of sponges with their microbial communities is a highly complex system, requiring interaction mechanisms and adaptation on both sides. The microbiome seems to rely on eukaryotic-like protein domains, such as ankyrins, modifications of the lipopolysaccharide structure, CRISPR-Cas, toxin-antitoxin, and restriction-modification systems, as well as secondary metabolism to communicate with the host and within the microbial community, evade phagocytosis, and defend itself against foreign DNA. Secondary metabolites produced by certain symbionts may even defend the entire holobiont against predators. On the other hand, the immune system of the sponge itself has evolved to discriminate not only between self and nonself but also between its associated microbiota and foreign microbes, such as food bacteria. Sponge holobionts are inextricably dependent on the surrounding environmental conditions due to their sessile nature. Thus, we discuss the link between environmental stress and sponge disease and dysbiosis, with a particular focus on the holobiont’s response to ongoing global change. While some species may be the “winners of climate change,” other species are adversely affected, e.g., by metabolic and immune suppression, as well as microbiome shifts resulting in loss of symbiotic functions. Hence, a much better understanding of sponge holobionts and the underlying molecular mechanisms of host-microbe interaction is required before the fate of sponge holobionts in a changing ocean can finally be validated.