Cnidarian-Microbe Interactions and the Origin of Innate Immunity in Metazoans

Abstract

Most epithelia in animals are colonized by microbial communities. These resident microbes influence fitness and thus ecologically important traits of their hosts, ultimately forming a metaorganism consisting of a multicellular host and a community of associated microorganisms. Recent discoveries in the cnidarian Hydra show that components of the innate immune system as well as transcriptional regulators of stem cells are involved in maintaining homeostasis between animals and their resident microbiota. Here I argue that components of the innate immune system with its host-specific antimicrobial peptides and a rich repertoire of pattern recognition receptors evolved in early-branching metazoans because of the need to control the resident beneficial microbes, not because of invasive pathogens. I also propose a mutual intertwinement between the stem cell regulatory machinery of the host and the resident microbiota composition, such that disturbances in one trigger a restructuring and resetting of the other.

Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

“…The cnidarian Hydra is a useful model to characterize a barrier epithelium, innate immune responses, tissue homeostasis and host-microbe interactions Bosch, 2007, 2010;Bosch et al, 2009;Fraune et al, 2009;Franzenburg et al, 2012;Bosch, 2013;Franzenburg, 2013b). Whereas polyps are colonized by a 'low-complexity' microbiota, the holobiont forms a highly specific ecosystem (Fraune and Bosch, 2007;Franzenburg et al, 2013b) that is similar between laboratory-raised animals and animals being taken from the wild (Fraune and Bosch, 2007).…”

“…This receptor complex activation then triggers the innate immune response that involves the production of a variety of immune effector genes (Franzenburg et al, 2012). Antimicrobial peptides are major components of the innate immune system of Hydra (Augustin et al, 2009a;Bosch et al, 2009;Bosch, 2013). The expression of selective antimicrobial peptides is critical for colonization by stable and species-specific bacterial communities Franzenburg et al, 2013b).…”

Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates

“…There is a growing appreciation that specific bacteria direct diverse animal developmental processes, including light organ development in the Hawaiian bobtail squid and immune system development and maturation in organisms as diverse as cnidaria and mammals (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). However, the multicellularity of animals and the complex communities of bacteria with which they often interact hinder the complete characterization of many hostmicrobe dialogues.…”

Mechanisms of Immune Responses in Cnidarians

“…Cnidarians have an immense capacity to regenerate their tissues as a consequence of the continuous proliferation of stem cells (Fautin, 2002); this could be considered as an additional arm of immune defense in these organisms since the cells infected intracellular parasites are quickly removed in a programmed way (apoptotic processes) and they are immediately replaced by non infected cells (Augustin et al, 2011). Cnidarians posses a complex set of symbiotic bacteria inhabiting the epithelial surfaces that compete with potential pathogens to colonize the tissues (Bosch, 2013). Alterations in the structure of the symbiotic bacterial communities due to environmental changes, might promote the proliferation of opportunistic microorganisms that can cause disease (Cárdenas et al, 2012).…”

“…Other protease inhibitors, the kunitz-type protease inhibitor and the alpha-2-macroglobulin, have been identified in anemones and are thought to play a role in immunity by inactivating virulence factors from bacteria (Fujito et al, 2010;Kimura et al, 2009;Peigneur et al, 2011). AMPs have been identified in Hydra (Bosch, 2013) and in the coral P. damicornis (Vidal-Dupiol et al, 2011). In the latter, the AMP is called damicornin, and it is expressed in the ectodermal granular cells and displays antimicrobial activity in vitro against Gram-positive bacteria and fungi (Vidal-Dupiol et al, 2011).…”