Iron limitation reduces diatom carbon flow to bacteria through shifts in exometabolite consumption

Abstract

Iron is required for photosynthesis and thus affects carbon fixation rates in widespread aquatic regions where availability is limited. Turnover of aquatic photosynthetically derived fixed carbon is largely constrained by bacterial activity, but it is unknown how algal iron limitation alters dissolved organic matter composition and subsequent processing through the microbial loop. We examined a bacterial community dependent on carbon from the diatom Phaeodactylum tricornutum to investigate how iron limitation alters bacterial carbon processing. By quantifying activity at single-cell-resolution with nanoSIMS, we found that iron limitation led to a 43% reduction in carbon-fixation but an 80% reduction in carbon transfer into bacterial biomass. Ultra-high-resolution exometabolomics revealed that iron limitation led to bacterial consumption of less labile compounds including aromatics, specific lipids, and nucleobases. A population of bacteria specific to the iron-deplete condition exhibited high anabolic activity yet low incorporation of newly fixed carbon, supporting a shift to consumption of compounds with longer residence times. From metagenome assembled genomes we identified candidate taxa and gene pathways responsible for this carbon processing shift. These results provide a mechanistic link between decreased carbon flow to bacteria under iron limitation and consumption of less labile exometabolites responsible for this decreased flow. This has implications for predicting organic matter composition and turnover in iron deplete surface oceans and manipulating algal-bacterial interactions in engineered systems.