Reduction-dependent siderophore assimilation in a model pennate diatom

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Abstract
Iron uptake by diatoms is a biochemical process with global biogeochemical implications. In large regions of the surface ocean diatoms are both responsible for the majority of primary production and frequently experiencing iron limitation of growth. The strategies used by these phytoplankton to extract iron from seawater constrain carbon flux into higher trophic levels and sequestration into sediments. In this study we use reverse genetic techniques to target putative iron-acquisition genes in the model pennate diatom Phaeodactylum tricornutum. We describe components of a reduction-dependent siderophore acquisition pathway that relies on a bacterial-derived receptor protein and provides a viable alternative to inorganic iron uptake under certain conditions. This form of iron uptake entails a close association between diatoms and siderophore-producing organisms during low-iron conditions. Homologs of these proteins are found distributed across diatom lineages, suggesting the significance of siderophore utilization by diatoms in the marine environment. Evaluation of specific proteins enables us to confirm independent iron-acquisition pathways in diatoms and characterize their preferred substrates. These findings refine our mechanistic understanding of the multiple iron-uptake systems used by diatoms and help us better predict the influence of iron speciation on taxa-specific iron bioavailability. Significance Diatoms can access inorganic iron with remarkable efficiency, but this process is contingent on carbonate ion concentration. As ocean acidification reduces carbonate concentration, inorganic iron uptake may be discouraged in favor of carbonate-independent uptake. We report details of an iron assimilation process that needs no carbonate but requires exogenous compounds produced by cooccurring organisms. We show this process to be critical for diatom growth at high siderophore concentrations, but ineffective at acquiring iron from low-affinity organic chelators or lithogenic particulates. Understanding the caveats associated with iron source preference in diatoms will help predict the impacts of climate change on microbial community structure in high-nitrate low-chlorophyll ecosystems.
Funding Information
  • National Science Foundation (NSF-OCE-1756884)
  • National Science Foundation (NSF-OCE-1756860)
  • National Science Foundation (NSF-MCB-1818390)
  • U.S. Department of Energy (DE-SC0018344)
  • Gordon and Betty Moore Foundation (GBMF3828)
  • Gordon and Betty Moore Foundation (GBMF5006)
  • Czech Science Foundation (15-17643S)

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