Fe(II) Speciation Regulates Microbial Metabolic Reprogramming and Phototrophic Fe(II) Mineralization in Rhodopseudomonas palustris SX2

Abstract

Phototrophic iron mineralization (PIM) is a keystone biogeochemical process linking anoxic iron redox transformations to carbon sequestration. Although PIM is widely documented, how Fe(II) speciation impacts cell physiology and thus causes divergent mineralization phenotypes remains poorly understood. In this study, we systematically investigated the physiological, mineralogical, and molecular responses of a newly isolated photoferrotroph, Rhodopseudomonas palustris SX2, exposed to uncomplexed Fe(II) [Fe(II) without OM] versus organically complexed Fe(II) [Fe(II)-OM] under anoxic and illuminated conditions. We demonstrate that distinct Fe(II) speciation drives divergent metabolic reprogramming for rapid metabolic adaptation and phototrophic biomineralization phenotypes. Fe(II) without OM triggered cell-surface encrustation and activated stress-mitigation and metal-efflux systems, whereas Fe(II)-OM stimulated the formation of discrete intracellular iron nanoparticles while upregulating photosynthetic light harvesting and autotrophic CO2 fixation. Furthermore, genetic knockout and complementation confirmed that the pioABC operon constitutes the indispensable electron conduit driving Fe(II) oxidation across both speciation regimes, with organic complexation significantly enhancing its transcriptional activation. Our findings reveal how metabolic adaptation driven by Fe(II) speciation dictates the spatial distribution of biogenic iron minerals and regulates the efficiency of coupled carbon sequestration in anoxic ecosystems.