An ancient lysozyme in placozoans participates in acidic extracellular digestion

TL;DR

A study reveals that placozoans have an ancient lysozyme involved in digestion and immunity, which originated from a bacterial gene transfer to early animals.

Contribution

The study identifies a functional lysozyme in placozoans and traces its evolutionary origin to a horizontal gene transfer event from bacteria.

Findings

PLys is highly active and produced by the ventral epithelium of Trichoplax sp. H2.

PLys contains a unique cysteine-rich domain that stabilizes the protein.

Structure-based phylogenetics shows metazoan GH23 lysozymes originated from a bacterial horizontal gene transfer.

Abstract

Lysozymes are an essential part of immunity and nutrition in metazoans, degrading bacterial cell walls via the hydrolysis of peptidoglycan. Although various lysozymes have been reported for higher animals, the origin of animal lysozymes remains elusive as they seem to be lacking in all early branching phyla. In this study, we investigated a putative goose-type lysozyme (PLys, glycoside hydrolase family 23, GH23) of the placozoan Trichoplax sp. H2. We show that PLys is highly active and primarily produced by cells of the placozoan ventral epithelium. PLys contains a non-conserved cysteine-rich domain N-terminal of the GH23 lysozyme domain, which stabilizes the protein and is truncated during maturation. Using a pH-sensitive fluorescence reporter, we show that Trichoplax sp. H2 acidifies its temporary feeding grooves pulsatively during digestive events close to the optimum pH for PLys activity. To elucidate the evolutionary origin of the metazoan GH23 lysozyme family, we applied structure-based phylogenetics to show that the metazoan g-type GH23 lysozymes 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 acting as first animal lysozyme and a key component in the antibacterial arsenal since early animal evolution.

Molecular and phylogenetic characterization of a placozoan lysozyme conserved in early-branching metazoans highlights the importance of horizontal gene transfer for metazoan evolution

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