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Evolution, ecology, and mechanisms of heme uptake in the marine Roseobacter lineage

This paper is available in a repository.
This paper is available in a repository.

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Abstract

The sources, transformations, and ultimate fate of heme and hemoproteins in seawater are poorly understood. The marine Roseobacters, an abundant and cosmopolitan bacterial lineage, are frequently found in environmental niches where heme concentrations are likely to be greatest. Here we show that in the Roseobacter group, heme uptake genes represent the most common strategy for organic-iron acquisition and are highly conserved with respect to synteny, sequence similarity, and transcription factor binding. We also argue that Roseobacters specialized to use heme as an iron source after genome divergence by way of horizontal gene transfer. We show that heme uptake genes of a model Roseobacter, Ruegeria sp. TM1040, are co-transcribed as an operon and are upregulated under iron stress. The insertional inactivation of a predicted TonB dependent outer membrane receptor in the heme uptake operon results in the inability of TM1040 to grow on heme as an iron source. Our results identify and confirm genes responsible for heme uptake in a model Roseobacter strain and highlight heme uptake as the dominant organic-iron uptake pathway within the rest of the lineage.