Iron limitation alters diatom carbon flow through shifts in microbiome exometabolite consumption

Abstract

Iron is required for photosynthesis, and thus affects biogeochemical cycling in widespread regions where its availability is limited. Turnover of aquatic photosynthetically-derived carbon is largely constrained by bacterial activity, but we lack a mechanistic understanding of how iron limitation influences this activity. We examined a bacterial enrichment community dependent on carbon from the diatom Phaeodactylum tricornutum to investigate how iron limitation alters the flow of carbon to bacteria, and exometabolite and community composition. Using stable isotope tracing, we quantified diatom exudate incorporation with single-cell-resolution. We identified a population of bacteria under iron limitation with high metabolic activity yet low incorporation of newly-fixed diatom carbon, indicating a shift in metabolism relative to the iron-replete control. Ultra-high-resolution exometabolomics revealed bacterial consumption of aromatics, lipid-like compounds, and purines and pyrimidines occurred under iron-limitation, when these compounds also exhibited increased exudation. We identified gene pathways for utilization of these compounds in taxa with increased abundance under iron limitation which may be responsible for carbon flow shifts. These results provide a mechanistic link between iron-limitation driven shifts in exudate composition and flow of carbon to the microbiome. This has important implications for predicting carbon flow in surface oceans and manipulating algal-bacterial interactions in engineered systems.