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.

Mesoglea Extracellular Matrix Reorganization during Regenerative Process in Anemonia viridis (Forskål, 1775)

“…Matrix metalloproteinases (MMPs) are a family of endopeptidases collectively able to degrade the components of the extracellular matrix. They play important roles in propeptides and collagen fibril formation and normal tissue remodeling, embryogenesis, angiogenesis, and wound healing [ 27 , 44 ].…”

“…Unlike the freshwater polyp Hydra, where regeneration is based on three distinct populations of multipotent stem cells, the I-cells, the ectodermal and endodermal epithelial cells [ 19 , 20 , 21 , 22 , 23 ], in anthozoans, another type of undifferentiated cell, called the amoebocyte, regulates this process [ 24 , 25 , 26 , 27 ]. These agranular hyaline cells are scattered in the mesoglea and can differentiate into fibroblast-like cells, characterized by extended pseudopodia and by the ability to control extracellular matrix production and collagen deposition [ 24 ].…”

Stem Cells and Innate Immunity in Aquatic Invertebrates: Bridging Two Seemingly Disparate Disciplines for New Discoveries in Biology

“…Innate immunity in aquatic invertebrates, as in the vertebrates, relies on recognition elements (their nature not yet disclosed in most taxa), tightly associated with a wide range of effector mechanisms. While many prominent properties of innate immunity systems are shared by all multicellular organisms (40)(41)(42)(43)(44)(45)(46), the evolutionary origin remains poorly understood, as well as the roles of stem cells in immunological pathways of aquatic invertebrates (47,48). Here, we present information on the relationships between stem and immune cells deriving from research on selected taxa of aquatic invertebrates.…”

“…One such example is the colonial tunicate B. schlosseri, where populations from several sites, worldwide, revealed 80 to 300 allorecognition alleles at the fusibility locus/site (165)(166)(167)(168). Indeed, while no homology has been established between marine invertebrates and vertebrates allorecognition genes, and not even among those of different invertebrate species (47,(169)(170)(171), a wide range of marine invertebrates, including sponges, cnidarians, bryozoans, and ascidians, reveal allorecognition competencies that represent high specificity and accuracy (44,172,173), also reflecting highly conserved effector mechanisms for innate immunity in the animal kingdom (40,(42)(43)(44)46). The discovery of specific and complex non-transitive hierarchies in marine invertebrates (174)(175)(176) is dictated by a variety of effector mechanisms that are tailored to recognize different conspecifics (177).…”

Ancient Immunity. Phylogenetic Emergence of Recognition-Defense Mechanisms

“…The next review [ 5 ] provides an exhaustive description of cnidarian immunity, with particular focus on anthozoans. Cnidarians are non-bilaterian animals lacking an internal circulatory system and their immunity relies mainly on epithelial cells.…”