Placozoan fiber cells: mediators of innate immunity and participants in wound healing.

Placozoa is a phylum of non-bilaterian marine animals. These small, flat organisms adhere to the substrate via their densely ciliated ventral epithelium, which mediates mucociliary locomotion and nutrient uptake. They have only six morphological cell types, including one, fiber cells, for which functional data is lacking. Fiber cells are non-epithelial cells with multiple processes. We used electron and light microscopic approaches to unravel the roles of fiber cells in Trichoplax adhaerens, a representative member of the phylum. Three-dimensional reconstructions of serial sections of Trichoplax showed that each fiber cell is in contact with several other cells. Examination of fiber cells in thin sections and observations of live dissociated fiber cells demonstrated that they phagocytose cell debris and bacteria. In situ hybridization confirmed that fiber cells express genes involved in phagocytic activity. Fiber cells also are involved in wound healing as evidenced from microsurgery experiments. Based on these observations we conclude that fiber cells are multi-purpose macrophage-like cells. Macrophage-like cells have been described in Porifera, Ctenophora, and Cnidaria and are widespread among Bilateria, but our study is the first to show that Placozoa possesses this cell type. The phylogenetic distribution of macrophage-like cells suggests that they appeared early in metazoan evolution.

Innate immunity in the simplest animals - placozoans.

BACKGROUND: Innate immunity provides the core recognition system in animals for preventing infection, but also plays an important role in managing the relationship between an animal host and its symbiont. Most of our knowledge about innate immunity stems from a few animal model systems, but substantial variation between metazoan phyla has been revealed by comparative genomic studies. The exploration of more taxa is still needed to better understand the evolution of immunity related mechanisms. Placozoans are morphologically the simplest organized metazoans and the association between these enigmatic animals and their rickettsial endosymbionts has recently been elucidated. Our analyses of the novel placozoan nuclear genome of Trichoplax sp. H2 and its associated rickettsial endosymbiont genome clearly pointed to a mutualistic and co-evolutionary relationship. This discovery raises the question of how the placozoan holobiont manages symbiosis and, conversely, how it defends against harmful microorganisms. In this study, we examined the annotated genome of Trichoplax sp. H2 for the presence of genes involved in innate immune recognition and downstream signaling. RESULTS: A rich repertoire of genes belonging to the Toll-like and NOD-like receptor pathways, to scavenger receptors and to secreted fibrinogen-related domain genes was identified in the genome of Trichoplax sp. H2. Nevertheless, the innate immunity related pathways in placozoans deviate in several instances from well investigated vertebrates and invertebrates. While true Toll- and NOD-like receptors are absent, the presence of many genes of the downstream signaling cascade suggests at least primordial Toll-like receptor signaling in Placozoa. An abundance of scavenger receptors, fibrinogen-related domain genes and Apaf-1 genes clearly constitutes an expansion of the immunity related gene repertoire specific to Placozoa. CONCLUSIONS: The found wealth of immunity related genes present in Placozoa is surprising and quite striking in light of the extremely simple placozoan body plan and their sparse cell type makeup. Research is warranted to reveal how Placozoa utilize this immune repertoire to manage and maintain their associated microbiota as well as to fend-off pathogens.

The proto-MHC of placozoans, a region specialized in cellular stress and ubiquitination/proteasome pathways.

The MHC is a large genetic region controlling Ag processing and recognition by T lymphocytes in vertebrates. Approximately 40% of its genes are implicated in innate or adaptive immunity. A putative proto-MHC exists in the chordate amphioxus and in the fruit fly, indicating that a core MHC region predated the emergence of the adaptive immune system in vertebrates. In this study, we identify a putative proto-MHC with archetypal markers in the most basal branch of Metazoans--the placozoan Trichoplax adhaerens, indicating that the proto-MHC is much older than previously believed--and present in the common ancestor of bilaterians (contains vertebrates) and placozoans. Our evidence for a T. adhaerens proto-MHC was based on macrosynteny and phylogenetic analyses revealing approximately one third of the multiple marker sets within the human MHC-related paralogy groups have unique counterparts in T. adhaerens, consistent with two successive whole genome duplications during early vertebrate evolution. A genetic ontologic analysis of the proto-MHC markers in T. adhaerens was consistent with its involvement in defense, showing proteins implicated in antiviral immunity, stress response, and ubiquitination/proteasome pathway. Proteasome genes psma, psmb, and psmd are present, whereas the typical markers of adaptive immunity, such as MHC class I and II, are absent. Our results suggest that the proto-MHC was involved in intracellular intrinsic immunity and provide insight into the primordial architecture and functional landscape of this region that later in evolution became associated with numerous genes critical for adaptive immunity in vertebrates.