Evolutionary Dynamics of Matrix Metalloproteases with Collagenolytic Activity in Teleosts

TL;DR

This study explores how certain enzymes evolved in fish, revealing gene duplication events and different regulation patterns that could impact aquaculture.

Contribution

The study identifies the evolutionary origins and regulatory dynamics of collagenolytic matrix metalloprotease genes in teleost fish.

Findings

MMP11 and MMP13 genes in teleosts show duplication events linked to genome duplication.

Duplicated MMP genes in sea bream and sea bass exhibit stage- or tissue-specific expression.

Phylogenetic and synteny analyses reveal distinct evolutionary origins for MMP paralogs.

Abstract

Fish, like all animals, need enzymes that can break down and rebuild the material surrounding their cells. These enzymes, called matrix metalloproteases, are essential for growth, tissue repair, and defense against disease. Despite their importance, we know little about how the genes behind these enzymes evolved in fish, which make up the largest and most diverse group of vertebrates. In this study, we traced the history of the genes that produce collagen-degrading metalloproteases across different animals, with a focus on fish. We discovered that while some of these genes remain single copies, others were duplicated during fish evolution and kept their function. By studying two important farmed fish, Sparus aurata (gilthead sea bream) and Dicentrarchus labrax (European sea bass), we found that the duplicated genes are regulated differently at different developmental stages or in different tissues. Our findings provide new insights into the biology and evolution of fish and may help improve aquaculture practices by linking gene function to fish development and health.

Matrix metalloproteases (MMPs) are zinc-dependent endopeptidases that are critical for extracellular matrix (ECM) remodeling, with key roles in tissue development and repair, and immune responses. Despite their evolutionary and functional importance, the diversification and regulatory dynamics of MMPs genes in teleosts remain poorly understood. This study investigates the evolutionary history of MMPs with collagenolytic activity in the vertebrates with an emphasis on teleosts. Using comparative genomics and phylogenetics we identified conserved single-copy mmp2 and mmp9 genes and duplicated mmp11 and mmp13 paralogs in all non-salmonid teleosts. Phylogenetic and synteny analyses suggest that mmp11 paralogs originated from the teleost-specific genome duplication (TSGD), whereas the origin of mmp13 paralogs originated from a more complex evolutionary scenario. Protein domain analysis confirmed conserved catalytic motifs across species, supporting functional retention. The expression patterns of paralog genes were studied in two model marine teleosts, the Sparus aurata (gilthead sea bream) and Dicentrarchus labrax (European sea bass). Developmental and adult tissue transcriptome analyses revealed three major expression patterns among the paralogs: similar expression, stage-specific or tissue-specific expression. The overall data point to varied evolutionary dynamics of MMP genes in the teleosts, tracing their origin to different whole-genome duplication events. Expression profiles on paralog genes in model teleosts suggest regulatory sub-functionalization as the most possible fate of retained MMPs paralogs in teleosts following whole-genome duplication.

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