Microbes adapt to iron scarcity through siderophore production across the eastern tropical Pacific

Daniel Repeta, Woods Hole Oceanographic Institution, Department of Marine Chemistry and Geochemistry, Woods Hole, MA, United States, Rene Boiteau, Woods Hole Oceanographic Institution, Woods Hole, MA, United States, Daniel Richard Mende, University of Hawaii at Manoa, C-MORE, Honolulu, HI, United States and Edward DeLong, University of Hawaiʻi at Mānoa, Department of Oceanography, School of Ocean and Earth Science and Technology, Honolulu, HI, United States
Abstract:
Iron regulates microbial growth and carbon fixation rates in vast regions of the ocean characterized by high nutrient and low chlorophyll (HNLC) concentrations. As competition for bioavailable iron in HNLC regions intensifies, microbial communities face tremendous selective pressure to develop efficient uptake and utilization strategies that access the strong organic ligands controlling iron bioavailability in these areas. Using liquid chromatography mass spectrometry, we found 27 unique iron complexes in surface waters sampled across the GEOTRACES eastern tropical Pacific zonal cruise track, with a clear trend in the abundance of different ligands across nutrient regimes. We identified siderophores, compounds produced by microbes under iron stress to facilitate iron uptake, as important components of iron ligands. Siderophore composition varied dramatically across the region, reflecting adaptive microbial strategies for acquiring iron. Concentrations of amphibactins, amphiphilic siderophores with cell membrane affinity, were low in coastal waters, but reached 9pM in HNLC waters, while ferrioxamine concentrations were higher in coastal and oligotrophic regions (1-2pM). These spatial changes in siderophore distributions represents adaptations used by marine microbes to acquire iron under different ecological conditions. To infer the potential ocean-wide contribution of amphibactins to microbial iron acquisition, we investigated the distribution of amphibactin synthesis genes in the recently published TARA Oceans metagenomic catalogue. We found amphibactin synthesis genes were present in other major iron-starved regions, suggesting that adaptations involving siderophore utilization likely impact global marine ecosystem composition and productivity.