Cnidarian Immunity and the Repertoire of Defense Mechanisms in Anthozoans

Abstract

Anthozoa is the most specious class of the phylum Cnidaria that is phylogenetically basal within the Metazoa. It is an interesting group for studying the evolution of mutualisms and immunity, for despite their morphological simplicity, Anthozoans are unexpectedly immunologically complex, with large genomes and gene families similar to those of the Bilateria. Evidence indicates that the Anthozoan innate immune system is not only involved in the disruption of harmful microorganisms, but is also crucial in structuring tissue-associated microbial communities that are essential components of the cnidarian holobiont and useful to the animal's health for several functions including metabolism, immune defense, development, and behavior. Here, we report on the current state of the art of Anthozoan immunity. Like other invertebrates, Anthozoans possess immune mechanisms based on self/non-self-recognition. Although lacking adaptive immunity, they use a diverse repertoire of immune receptor signaling pathways (PRRs) to recognize a broad array of conserved microorganism-associated molecular patterns (MAMP). The intracellular signaling cascades lead to gene transcription up to endpoints of release of molecules that kill the pathogens, defend the self by maintaining homeostasis, and modulate the wound repair process. The cells play a fundamental role in immunity, as they display phagocytic activities and secrete mucus, which acts as a physicochemical barrier preventing or slowing down the proliferation of potential invaders. Finally, we describe the current state of knowledge of some immune effectors in Anthozoan species, including the potential role of toxins and the inflammatory response in the Mediterranean Anthozoan Anemonia viridis following injection of various foreign particles differing in type and dimensions, including pathogenetic bacteria.

Keywords: Anthozoan; bioactive molecules; cnidarians; inflammatory response; innate immunity.

Figure 1

Cnidarian evolutionary history based on rRNA phylogenies.

Figure 2

General scheme of the main invertebrate immunity components identified within Anthozoans. TLR, TOLL-like receptor; C3 Complement protein; IL-1Rs, Interleuchin-like; MyD88, myeloid differentiation primary-response protein 88; transcription factors NF-κB; C3, Complement protein; MASPs, mannose binding lectin-associated serine proteases; MACPF, Membrane-attack complex–perforin protein; FAK, focal adhesion kinases; AMPs, antimicrobial peptides; ROS, reactive oxygen species.

Figure 3

Plaque of lysis assay from cells isolated from Actinia equina against rabbit erythrocytes. Lysis plaques in a Cunningham–Szenberg chamber were observed when cells were mixed with target erythrocytes. Granulocytes were cytotoxic cells. Scale bar: 100 µm.

Figure 4

Anatomy of Anemonia viridis. Gomory stain of tentacles histological section (M: Mesoglea, Sy: Symbiont, Sp: Spyrocysts, Muc: Mucocytes, Ci: Cilia, MF: Muscular fiber). Bar: 10 µm.

Figure 5

A. viridis color morphs based on pigment content. Specimens collected along the North Sicilian coast and maintained in the laboratory. The red (rustica variety) and green (viridis variety) pigment leakage is detectable after irradiation with ultraviolet light.

Figure 6

Morphology variation after bacterial infection in A. viridis. (A), Schematic model of anatomy and injection site, swelling and reaction (B), Reaction zone (C), rejection and swelling of animal body 24 h after injection of suspensions of various heat-killed bacteria in (inset) the reaction after E. coli injection (D), A. viridis Gomori stain histological section (E), The original figure was produced for the study published by Trapani et al., [135]. The modified figure is consistent with the topic of the review.