Metadata and Data for https://doi.org/10.1128/mSystems.00124-16

In this study we investigated the molecular basis of heme transport, an organic iron acquisition pathway, in phytoplankton-associated Roseobacter bacteria and explored the potential role of bacterial heme uptake in the marine environment. We searched 153 Roseobacter genomes and found that nearly half contained putative complete heme transport systems with near identical synteny. We also examined a publicly available co-culture transcriptome and found that the Roseobacter strain, Sulfitobacter sp. SA11, strongly downregulated a putative heme transport gene cluster during mutualistic growth with a marine diatom suggesting that the regulation of heme transport might be influenced by host cues. We generated a mutant of the phytoplankton-associated Roseobacter strain Ruegeria sp. TM1040 by insertionally inactivating its homolog of the TonB-dependent heme transporter hmuR and confirmed the role of this gene in the uptake of heme and hemoproteins. We performed competition experiments between iron-limited wild type and mutant TM1040 strains and found that the wild type maintains a growth advantage when competing with the mutant for iron compounds derived solely from lysed diatom cells. Heme transport systems were largely absent from public marine metagenomes and metatranscriptomes, suggesting that marine bacteria with the potential for heme transport likely have small standing populations in the free-living bacterioplankton. Heme transport is likely a useful strategy for phytoplankton-associated bacteria because it provides direct access to components of the host intracellular iron pool after lysis.