Origin of the Metazoan Immune System: Identification of the Molecules and Their Functions in Sponges

Abstract

During the evolutionary transition to Metazoa, cell-cell- as well as cell-matrix recognition molecules have been formed, which made a further step in evolution possible, the establishment of an immune system. Sponges [Porifera] represent the oldest still extant metazoan phylum and consequently testify to major features of the common metazoan ancestor, the Urmetazoa. Most studies with respect to evolution and phylogeny in sponges have been performed with the marine demosponges Suberites domuncula and Geodia cydonium. These animals possess effective defense systems against microbes and parasites which involve engulfment of bacteria into specific cells, but also signal transduction pathways which actively kill bacteria. Among those is the LPS-mediated pathway, with the stress-responsive kinases. In addition, sponges are provided with an interferon-related system, with the (2-5)A synthetase as controlling enzyme. Transplantation studies have been performed on tissue, as well as at the cellular level ("mixed sponge cell reaction assay") which demonstrate the complex molecular strategy by which sponges respond to allogeneic- and/or autogeneic signals. Among the molecules involved in histo(in)compatibility response of sponges, cytokines e.g., the allograft inflammatory factor 1, have been identified which control rejection of allografts. Furthermore, transcription factors, with Tcf-like factor as an example, have been identified which very likely control gene expression during histocompatibility reactions. The immune reactions in sponges can be modulated by FK506, a drug which has been successfully used as immunosuppressant in humans. One further surprising finding is the fact that G. cydonium has several molecules containing polymorphic Ig-like domains of the variable type. It is concluded that the successful evolutionary transition to the Metazoa, with the sponges as the oldest still extant phylum, and the subsequent rapid radiation into the other metazoan phyla, became possible because of the acquisition of modular molecules, involved in cell adhesion and the immune system.

Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

“…Microorganisms can be either acquired from the surrounding sea water during filter-feeding process of sponges or transferred from the parental sponges to progeny through reproductive stages. The former (horizontal or environmental transmission) requires certain degrees of recognition, possibly via the innate immune system in sponges (Mü ller and Mü ller, 2003), to differentiate symbionts from food microbes. Under this scenario, there would be some overlap between the microbes in the surrounding sea water and sponges.…”

Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida

“…It may be assumed that microorganisms capable of association with sponges are present in the surrounding seawater and environment, but at abundances below the detection limit of currently available methods (Mü ller and Mü ller, 2003). Therefore, as anaerobic bacteria are not major components of the bacterial communities of seawater, resuspended sediment particles are a likely source for these and other microbiota.…”

Cyclosporin A Suspends Transplantation Reactions in the Marine SpongeMicrociona prolifera

“…When tissues from different individuals of a given sponge species are brought into contact, they either fuse or reject through cellular events similar to those observed in vertebrate grafts (7). Sponges possess elements involved in transplantation immunity that are key components of mammalian innate immunity (8). These include molecules containing scavenger receptor cysteine-rich domains (9), TLRs (10), the 2Ј,5Ј-oligoadenylate synthetase (11), cytokine-like molecules (12), and also factors similar to those produced by cytokine-responsive macrophage molecules such as the allograft inflammatory factor 1 (13).…”

“…Despite this incipient knowledge at the molecular level of some components of the allogeneic recognition system in sponges (8), little is known about the actual underlying mechanism or the cells involved in the process. Sponges lack lymphocytes and the existence of immune cells in this phylum has been object of debate (30,31).…”