Comparative genomics reveals expanded cell-surface signaling and siderophore scavenging repertoires in Pectobacterium

ABSTRACT Iron acquisition in gram-negative bacteria relies on TonB-dependent receptors (TBDRs), some of which initiate cell-surface signaling (CSS) by activating extracytoplasmic function (ECF) sigma factors that induce cognate transport pathways. Although well characterized in Pseudomonas , CSS systems remain poorly explored in plant-associated bacteria. Surveying 6,847 plant-associated bacterial genomes revealed near-ubiquitous CSS systems in Pseudomonas and Pectobacterium , with markedly lower strain-to-strain variation in the latter. In 902 high-contiguity Pectobacteriaceae genomes, Pectobacterium averaged 5.03 CSS modules per genome, compared with 0.67 in Dickeya , despite their shared soft-rot lifestyle. De novo clustering identified 14 distinct CSS systems across the family, with nine found in Pectobacterium . The ferredoxin receptor gene fusA was conserved in 572 of 586 Pectobacterium genomes; however, only 126 carried fusA under CSS regulation. These strains were phylogenetically dispersed but formed a single fusA clade, a pattern consistent with co-acquisition of the receptor and regulator as a transferable module. Pectobacterium also encoded a more diverse repertoire of siderophore receptors than related taxa, suggesting broader potential for siderophore utilization across bacterial lineages. Notably, the predicted amonabactin-like biosynthetic gene cluster and its putative cognate TBDR were highly conserved within Pectobacterium but rare elsewhere in the family, supporting its potential role in the endogenous siderophore system in the genus. These findings reveal an expanded genomic repertoire of CSS systems and siderophore receptors in Pectobacterium , providing a framework for investigating their roles in environmental sensing and iron acquisition. IMPORTANCE Bacteria often use cell-surface signaling systems to sense environmental cues and coordinate the uptake of substrates that cannot freely cross the outer membrane, including siderophores and host-derived proteins. Through comparative genomic analysis, we demonstrate that Pectobacterium harbors one of the richest and most diverse repertoires of these cell-surface signaling systems among plant-associated bacteria. Despite similar lifestyles, its repertoire far exceeds that of other Pectobacteriaceae and reveals extensive predicted siderophore producer–scavenger relationships within the genus and across the family. These expanded signaling and siderophore acquisition systems in Pectobacterium may contribute to its environmental adaptability and ecological versatility by broadening opportunities for nutrient acquisition and interactions with surrounding microbial communities.