Metagenomic Profiling and Genome-Centric Analysis Reveal Iron Acquisition Systems in Cheese-Associated Bacteria and Fungi.

Cheese microbial communities are composed of diverse interacting microorganisms, including both inoculated and non-inoculated strains. One limiting factor for microbial growth on cheese surfaces is iron availability. To better understand the role of iron acquisition in cheese microbial ecology, we investigated the diversity and distribution of iron uptake systems across a wide range of cheeses. We analysed 136 metagenomes and 1400 genomes and Metagenome-Assembled Genomes (MAGs) from 44 French Protected Designation of Origin (PDO) cheeses. Using an updated set of Hidden Markov Models targeting iron acquisition genes, we identified a wide diversity of iron uptake systems. Siderophore biosynthesis and import systems were more prevalent in surface-associated species than in those from the cheese core. About 20 different siderophore biosynthesis pathways were detected, with desferrioxamine and enterobactin-type being the most prevalent. Genomic analyses revealed the main bacterial and fungal producers, including Glutamicibacter, Corynebacterium, Staphylococcus, and Penicillium. While siderophore biosynthesis pathways were found in a minority of MAGs, iron/siderophore import systems were widespread, suggesting the potential for cross-feeding interactions involving siderophores. These findings enhance our understanding of microbial interactions in cheese and open perspectives for improving ripening cultures by considering iron acquisition traits.