Control of Peripheral Light-Harvesting Complex Synthesis by a Bacteriophytochrome in the Aerobic Photosynthetic Bacterium Bradyrhizobium Strain BTAi1

Abstract

The recent sequence analysis of the photosynthetic and plant-symbiotic Bradyrhizobium sp. strain BTAi1 revealed the unexpected presence of a pucBA operon encoding the apoproteins of peripheral light-harvesting (LH) complexes. This pucBA operon is found close to a bacteriophytochrome gene (BphP3 B BTAi1 ) and a two-component transcriptional regulator gene (TF BTAi1 gene). In this study, we show that BphP3 B BTAi1 acts as a bona fide bacteriophytochrome and controls, according to light conditions, the expression of the pucBA operon found in its vicinity. This light regulatory pathway is very similar to the one previously described for chromo-BphP4 Rp in Rhodopseudomonas palustris and conducts the synthesis of a peripheral LH complex. This LH complex presents a single absorption band at low temperature, centered at 803 nm. Fluorescence emission analysis of intact cells indicates that this peripheral LH complex does not act as an efficient light antenna. One putative function of this LH complex could be to evacuate excess light energy in order to protect Bradyrhizobium strain BTAi1, an aerobic anoxygenic photosynthetic bacterium, against photooxidative damage during photosynthesis.Anoxygenic phototrophic bacteria have the ability to transform light energy into biochemical amenable energy for their growth and motion. The collection of light and its transformation into chemical energy are mediated by the so-called photosynthetic apparatus. This complex system is composed of three multimeric transmembrane protein complexes: the lightharvesting (LH) complexes, the photochemical reaction center (RC), and the cytochrome bc 1 complex located in the intracytoplasmic membrane. Light collected by the peripheral LH complexes is transferred first to the LH1 complex, which absorbs at around 870 nm, and then to the RC, where a charge separation occurs. This initiates a cyclic electron transfer between the RC and cytochrome bc 1 via electron carrier proteins in the periplasmic space and quinone molecules in the membrane. This cyclic electron transfer is coupled to the translocation of protons and to the formation of a proton motive force across the inner membrane, ultimately used for ATP synthesis. To optimize light collection, various peripheral LH complexes, coded by different pucBA genes, are expressed according to environmental conditions. In most cases, peripheral LH complexes absorb at 800 and 850 nm and are designated LH2. However, other peripheral LH complexes, which differ by their absorption properties and carotenoid content, have been described. At low light intensities and/or low temperatures, Rhodopseudomonas acidophila synthesizes an LH complex, designated LH3, which absorbs at 800 and 820 nm (4, 8). An atypical LH complex (LH4), presenting a single band around 805 nm, is synthesized by Rhodopseudomonas palustris cells when grown at a low light intensity (16).In general, the photosynthetic activity of anoxygenic phototrophic bacteria takes place under anaerobic or semiaerobic conditions, since the synthesis of the ph...

Comparative Genomics of Aeschynomene Symbionts: Insights into the Ecological Lifestyle of Nod-Independent Photosynthetic Bradyrhizobia

“…Unlike ORS278 strain, the PS apparatus of BTAi1 strain contains additional peripheral light-harvesting complex (LH2) encoded by a pucBA operon. The expression of this operon is also under the control of a bacteriophytochrome ( BBta_3080 ) found at the vicinity of the pucBA operon [ 26 ]. Interestingly, this gene organization is found in two of the other three photosynthetic strains (ORS375 and STM3809) that were studied, suggesting that the presence of LH2 complexes is rather frequent in PB strains.…”

Genomic insights into the versatility of the plant growth-promoting bacterium Azospirillum amazonense

“…B510 has two genes that code for distinct types of bacteriophytochromes [ 7 ], and Bradyrhizobium sp. possesses three bacteriophytochrome genes [ 68 ]. In plants, phytochromes regulate the metabolic response to the light environment, but a variety of functions is found in other organisms [ 69 ].…”

Pseudomonas syringae pv. syringae B728a Regulates Multiple Stages of Plant Colonization via the Bacteriophytochrome BphP1

“…Bacteriophytochromes have been found to regulate pigment production in D. radiodurans ( 7 ) and heat tolerance and pyocanin production in P. aeruginosa ( 9 ). In stem-nodulating Bradyrhizobium strains, bacteriophytochromes regulate a metabolic shift from chemoheterotrophy when cells are in soil to photoheterotrophy when cells are in stem nodules, thus allowing the cells to exploit a more energetically favorable form of metabolism when light is available ( 10 , 11 ). Although the bacteriophytochromes of Xanthomonas species lack the histidine kinase domain characteristic of those in other plant bacteria ( 12 ), these bacteriophytochromes were recently shown to suppress light-mediated phenotypes and contribute to the virulence of Xanthomonas campestris pv.…”