Iron oxidation is regulated by the two-component system, RegSR, and plays a role in photolithoheterotrophic growth in Rhodopseudomonas palustris

Abstract

Purple nonsulfur bacteria (PNSB) are metabolically versatile organisms generate energy through both aerobic and anaerobic respiration as well as anoxygenic photosynthesis. In many PNSB, the redox-sensing, two-component system RegBA is a global regulator of energy generating and consuming pathways, such as photosynthesis, carbon fixation, and nitrogen fixation, when cells are shifted from an aerobic to an anaerobic environment. However, in the PNSB Rhodopseudomonas palustris, the role of the RegBA homolog, RegSR, was unclear since global regulation of these same pathways involves the oxygen-sensing signal transduction system, FixJL-K, in R. palustris. Using RNA-seq analysis, we found that RegSR plays a role in regulating the operon pioABC, which encodes genes required for Fe(II) oxidation. We found that transcript levels of pioABC under photoheterotrophic conditions was dependent on the oxidation state of the carbon substrate and whether the cells were fixing nitrogen. We also found that R. palustris can carry out photolithoheterotrophic growth using Fe(II) oxidation when grown with the oxidized carbon substrate, malate, requiring regSR and pioABC. We present a model in which RegSR regulates pioABC in response to a cellular redox signal, allowing R. palustris to use Fe(II) oxidation to access more electrons when there is an increased cellular demand for reducing equivalents. Significance Mixotrophy is thought to be widespread in aquatic environments, yet little is understood about how mixotrophy affects biogeochemical cycles. Fe(II)-oxidizing anoxygenic phototrophs likely play an important role in iron cycling since they are thought to have thrived in the anoxic, iron-rich oceans of early Earth and can be found in both freshwater and marine environments. Although Fe(II) oxidation by anoxygenic phototrophs is largely studied in the context of photoautotrophic growth, these organisms can also grow photoheterotrophically. We present the first evidence linking photolithoheterotrophic growth using Fe(II) to the pathway required for photoautotrophic Fe(II) oxidation in an anoxygenic phototroph. Understanding this metabolism will be important for understanding how mixotrophic metabolism contributes to iron cycling in anoxic environments.