TonB-dependent Transporters of Fe-petrobactin in Marinobacter nauticus and Southern Ocean bacteria

Abstract

TonB-dependent transporters (TBDTs) play a central role in siderophore-mediated iron acquisition in the marine environment. However, assigning substrate specificity to TBDTs remains a major bottleneck in understanding the ecological and mechanistic roles of siderophore production and uptake. Here, we identify in Marinobacter nauticus two TBDTs, OptA and OptB, that share low sequence identity yet both mediate Fe-petrobactin uptake. Despite this functional overlap, they underlie distinct regulatory mechanisms, suggesting differential utilization under specific environmental conditions. Phylogenetic analyses indicate that OptA likely co-evolved with the petrobactin biosynthetic gene cluster, whereas OptB appears to have followed a distinct evolutionary trajectory, acquiring the capacity to import petrobactin as a xenosiderophore. Using resuscitated communities from the Southern Ocean, we further show that Fe-petrobactin stimulated prokaryotic growth. Based on amino acid similarity, we identified OptB-like transporters encoded in metagenomes and MAGs and show that taxa harbouring these transporters, such as Pseudoaltermonas, respond specifically to Fe-petrobactin addition. OptB-like transporters were also detected in environmental metagenomes from the Southern Ocean, whereas the petrobactin biosynthetic gene clusters were not, indicating that petrobactin primarily functions as a xenosiderophore in natural communities.