An ancient lysozyme in placozoans

Lysozymes are an essential part of nutrition and antibacterial immunity in metazoans, executing the breakdown of bacterial cell walls via the hydrolysis of peptidoglycan. Although various lysozymes have been reported for several bilaterian phyla, the origin of metazoan lysozymes remains elusive as they seem to be lacking in non-bilaterian animals. In this study, we investigated a putative goose-type lysozyme (PLys, glycoside hydrolase family 23, GH23) of the placozoan Trichoplax sp. H2 which we localized to gland cells of the ventral epithelium. N-terminal of the conserved GH23 lysozyme domain, PLys contains a non-conserved cysteine-rich domain. We could show a truncation of this N-terminal domain in the maturation process of PLys and a drastic increase in enzymatic activity at the cost of stability using recombinantly expressed physiological proteoforms of PLys. Phylogenetic analysis of GH23 lysozymes from all domains of life revealed a monophyletic radiation in animals. Based on structural comparisons and their distribution in the animal tree of life, metazoan g-type GH23 lysozymes appear to have originated from a horizontal gene transfer event from bacteria to an early pre-bilaterian ancestor. GH23 lysozymes have then been retained and expanded in many phyla, including Porifera, Cnidaria, Placozoa and chordates, acting as key component in the antibacterial arsenal since early metazoan evolution.