Distribution of siderophore gene systems on a Vibrionaceae phylogeny: Database searches, phylogenetic analyses and evolutionary perspectives

Abstract

Siderophores are small molecules synthesized and secreted by bacteria and fungi to scavenge iron. Extracellular ferri-siderohores are recognized by cognate receptors on the cell surface for transport over membranes. Several siderophore systems from <i>Vibrionaceae</i> representatives are known and well understood, e.g., the molecular structure of the siderophore, the biosynthesis gene cluster and pathway, and the gene expression pattern. Less is known about how these systems are distributed among the ~140 <i>Vibrionaceae</i> species, and which evolutionary processes contributed to the present-day distribution. In this work, we compiled existing knowledge on siderophore biosynthesis systems and siderophore receptors from <i>Vibrionaceae</i> and used phylogenetic analyses to investigate their organization, distribution, origin and evolution. Through literature searches, we identified nine different siderophore biosynthesis systems and thirteen siderophore receptors in <i>Vibrionaceae</i>. Homologs were identified by BLAST searches, and the results were mapped onto a Vibrionaceae phylogeny. We identified 81 biosynthetic systems distributed in 45 <i>Vibrionaceae</i> species and 16 unclassified <i>Vibrionaceae</i> strains, and 409 receptors in 89 Vibrionaceae species and 49 unclassified <i>Vibrionaceae</i> strains. The majority of taxa are associated with at least one type of siderophore biosynthesis system, some (e.g., aerobactin and vibrioferrin) of which are widely distributed in the family, whereas others (i.e., bisucaberin and vibriobactin) are found in one lineage. Cognate receptors are found more widespread. Phylogenetic analysis of three siderophore systems (piscibactin, vibrioferrin and aerobactin) show that their present-day distribution can be explained by an old insertion into <i>Vibrionaceae</i>, followed mainly by stable vertical evolution and extensive loss, and some cases of horizontal gene transfers. The present work provides an up to date overview of the distribution of siderophore-based iron acquisition systems in <i>Vibrionaceae</i>, and presents phylogenetic analysis of these systems. Our results suggest that the present-day distribution is a result of several evolutionary processes, such as old and new gene acquisitions, gene loss, and both vertical and horizontal gene transfers.