How to Detect and Disarm Microbial Attackers Antimicrobial Defense Reactions in the Freshwater Polyp Hydra and the Jellyfish Aurelia

Cnidaria are soft-bodied animals lacking migratory phagocytic cells, hemolymph, and impermeable barriers, such as a cuticle or an exoskeleton, resulting in seemingly high vulnerability to pathogens. The animals live in habitats containing myriads of microbes and are constantly exposed to them. Scattered amidst the microbes are potential pathogens - bacteria, viruses, or protists - capable of tissue destruction and functional impairment.

Recently (Bosch et al., in preparation) we showed that, in the absence of migratory phagocytic cells and protective layers, the epithelium of the freshwater polyp Hydra magnipapillata is remarkably well equipped to survive in an environment teeming with potential pathogens and to prevent infectious agents from entering the body. To find out how the host perceives infection, we used a combined biochemical and transcriptome analysis approach to identify proteins and genes involved in epithelial defense (Bosch et al., in preparation). We could show that, in Hydra, all innate immune responses are mediated by the epithelial cells. Following pathogen invasion, there is an activation of an inducible defense system marked by an increased expression of genes encoding antimicrobial peptides. One of them is Hydramacin-1, a basic eight cysteines containing a cationic 60-aa peptide with a calculated molecular mass of 7009 Da (Bosch et al., in preparation). Hydramacin-1 is expressed exclusively in the endodermal epithelium, inducible by microbial products, and an antimicrobial peptide with extraordinary high activity against Bacillus megaterium (Bosch et al., in preparation). In the absence of conventional Toll-like receptors (TLRs; Miller et al. 2007), a leucine-rich repeat (LRR) lacking putative transmembrane receptor with a highly conserved Toll/IL-1 receptor (TIR) domain responds to microbial signals and cell death-associated molecules and is required for antimicrobial peptide induction (Bosch et al., in preparation). Interestingly, the expression of host-defense genes is affected by nerve cells (Kasahara and Bosch 2003; Bosch et al., in preparation). The results revealed several novel facts concerning the evolution of innate immune reactions: (a) the ancestral system of host defense is the inducible expression of antimicrobial peptides, (b) the epithelium represents the ancient system of host defense, and (c) even at the base of eumetazoan evolution the expression of immune effector genes is affected by nerve cells, suggesting that the neuro-immuno connection may be as old as the nervous system. In other animal groups communication and reciprocal regulation between the nervous and immune systems have been proposed to be essential for the stability of the organism. So far, however, studies have focused either on the evolution of the immune system or on the evolution the nervous system (Brogden et al. 2005). Our study (Kasahara and Bosch 2003) showed for the first time that both systems evolved in close relation to each other together and that Hydra will provide insight in a phylogenetically old, intriguing system that has developed to cope effectively with infections of various types.

Most recently, a novel antimicrobial peptide was purified from the mesoglea of the jellyfish Aurelia aurita, one of the most common and widely recognized types of jellyfish found near the coasts in the Atlantic, Arctic, and Pacific Oceans (Ovchinnikova et al. 2006). Aurelin, a 40-residue antimicrobial peptide with a molecular mass of 4296.95 Da was shown to exhibit activity against Gram-positive (Listeria monocytogenes, strain EGD) and Gram-negative (Escherichia coli, strain ML-35p) bacteria. Its primary structure, including six cysteines forming three disulfide bonds, as well as the primary structure of its molecular precursor, consisting of a canonical signal peptide, anionic propiece, and a mature cationic part, resembles the common structural features of animal defensins (Ovchinnikova et al. 2006). However, the distribution of cysteine residues makes it also similar to the K+ channel-blocking toxins of sea anemones. Although aligning the aurelin and sea anemone toxin sequences shows rather moderate homology, Ovchinnikova et al. (2006) suggests that aurelin could be functionally related to the ShK-like toxins. Both the expression pattern as well as the in vivo function of aurelin remain to be clarified.

Similar to Hydra and jellyfish, corals also lack a physical barrier such as a hard exoskeleton. Although molecular and biochemical studies have not yet been published, there is evidence that corals depend on their anti-microbial mucus to remove and lyse bacterial invaders (Phillips 1963; Bigger and Hildemann 1982).

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