Potential siderophore-dependent mutualism in the harmful dinoflagellate Alexandrium pacificum (Group IV) and bacterium Photobacterium sp. TY1-4 under iron-limited conditions

Abstract

Specific bacterial species induce algal blooms by producing growth-promoting substances, such as siderophores, under iron-limited conditions. However, the molecular mechanisms underlying these effects remain poorly understood. This study investigates the interactions between the harmful dinoflagellate Alexandrium pacificum (Group IV) and siderophore-producing bacteria, with a focus on iron acquisition facilitated by bacterial siderophores. During algal bloom seasons in the South Sea of Korea, Photobacterium sp. TY1-4 was isolated, which enhances A. pacificum cell density under iron-deficient conditions, TY1-4 can use the sterile exudates from A. pacificum as the sole source of carbon, suggesting a mutualistic relationship. Transcriptomic and genomic analyses revealed siderophore-mediated redox-based signaling and non-reductive pathways enhancing iron bioavailability. Photobacterium sp. TY1-4 initiates siderophore production through quorum sensing, whereas A. pacificum utilizes specific receptors and transporters for hydroxamate-type siderophores (ApFHUA and ApFHUC) to uptake iron. Three redox key iron-uptake genes were also identified in A. pacificum: membrane-bound ferroxidase ApFET3, high-affinity iron permease ApFTR1, and ferric-chelate reductases/oxidoreductases ApFRE1, with transcription levels inversely related to bioavailable iron. Increased iron bioavailability mediated by siderophores alleviates iron stress in A. pacificum, supporting its growth in iron-scarce environments. Additionally, A. pacificum co-cultured with Photobacterium sp. TY1-4 synthesized high-toxicity STXs, including GTX4, GTX2, and STX. These findings highlight the critical role of bacterial siderophores in iron binding and their potential impact on harmful algal bloom dynamics.