Abstract
Photosynthetic bacteria have to deal with the risk of photooxidative stress that occurs in presence of light and oxygen due to the photosensitizing activity of (bacterio-) chlorophylls. Facultative phototrophs of the genus Rhodobacter adapt the formation of photosynthetic complexes to oxygen and light conditions, but cannot completely avoid this stress if environmental conditions suddenly change. R. capsulatus has a stronger pigmentation and faster switches to phototrophic growth than R. sphaeroides. However, its photooxidative stress response has not been investigated. Here, we compare both species by transcriptomics and proteomics, revealing that proteins involved in oxidation–reduction processes, DNA, and protein damage repair play pivotal roles. These functions are likely universal to many phototrophs. Furthermore, the alternative sigma factors RpoE and RpoHII are induced in both species, even though the genetic localization of the rpoE gene, the RpoE protein itself, and probably its regulon, are different. Despite sharing the same habitats, our findings also suggest individual strategies. The crtIB-tspO operon, encoding proteins for biosynthesis of carotenoid precursors and a regulator of photosynthesis, and cbiX, encoding a putative ferrochelatase, are induced in R. capsulatus. This specific response might support adaptation by maintaining high carotenoid-to-bacteriochlorophyll ratios and preventing the accumulation of porphyrin-derived photosensitizers.
Highlights
Microbes in aquatic habitats need to adapt to frequent changes in environmental parameters like temperature, O2-saturation, or light conditions
While phototrophic bacteria can take advantage of pigment-protein complexes to use light energy for ATP production, they face the special challenge of photooxidative stress: chlorophylls can act as photosensitizers and transfer energy to the ground state triplet oxygen (3O2), causing a spin conversion in the π*2p orbital that generates highly reactive singlet oxygen (1O2)
When cultures of the two species were kept under microaerobic conditions in the dark, the growth behavior was nearly identical. a shift from high oxygen to phototrophic conditions with 60 W·m−2 white light revealed a remarkably faster adaption process for R. capsulatus, i.e., entering the exponential growth after the shift took ~4 h for R. capsulatus but ~21 h for R. sphaeroides (Figure 1B)
Summary
Microbes in aquatic habitats need to adapt to frequent changes in environmental parameters like temperature, O2-saturation, or light conditions. While phototrophic bacteria can take advantage of pigment-protein complexes to use light energy for ATP production, they face the special challenge of photooxidative stress: (bacterio-) chlorophylls can act as photosensitizers and transfer energy to the ground state triplet oxygen (3O2), causing a spin conversion in the π*2p orbital that generates highly reactive singlet oxygen (1O2). Due to a high metabolic versatility, they do not rely on photosynthesis for ATP production, but can perform aerobic or anaerobic respiration or fermentation. They do not form photosynthetic complexes at high oxygen concentrations, and at intermediate oxygen concentration, light inhibits the accumulation of pigment-protein complexes [2,3], which reduces the risk of photooxidative stress. Several protein regulators, including redox-responsive factors, photoreceptors, and even proteins with dual-sensing function like AppA [2], and RNA regulators [4,5], contribute to the regulated formation of photosynthetic complexes
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