Photoresponses in Rhodobacter sphaeroides: role of photosynthetic electron transport

Abstract

Rhodobacter sphaeroides responds to a decrease in light intensity by a transient stop followed by adaptation. There is no measurable response to increases in light intensity. We confirmed that photosynthetic electron transport is essential for a photoresponse, as (i) inhibitors of photosynthetic electron transport inhibit photoresponses, (ii) electron transport to oxidases in the presence of oxygen reduces the photoresponse, and (iii) the magnitude of the response is dependent on the photopigment content of the cells. The photoresponses of cells grown in high light, which have lower concentrations of light-harvesting photopigment and reaction centers, saturated at much higher light intensities than the photoresponses of cells grown in low light, which have high concentrations of light-harvesting pigments and reaction centers. We examined whether the primary sensory signal from the photosynthetic electron transport chain was a change in the electrochemical proton gradient or a change in the rate of electron transport itself (probably reflecting redox sensing). R. sphaeroides showed no response to the addition of the proton ionophore carbonyl cyanide 4-trifluoromethoxyphenylhydrazone, which decreased the electrochemical proton gradient, although a behavioral response was seen to a reduction in light intensity that caused an equivalent reduction in proton gradient. These results strongly suggest that (i) the photosynthetic apparatus is the primary photoreceptor, (ii) the primary signal is generated by a change in the rate of electron transport, (iii) the change in the electrochemical proton gradient is not the primary photosensory signal, and (iv) stimuli affecting electron transport rates integrate via the electron transport chain.

Characterization of the chemotaxis protein CheW from Rhodobacter sphaeroides and its effect on the behaviour of Escherichia coli

“…Previously it has been shown, in that chemotaxis to the dominant chemoattractants such as succinate and propionate requires transport and partial metabolism Ingham and Armitage, 1987;Jacobs et al, 1995). It is possible, therefore, that the second chemosensory pathway may sense the metabolic state of the cell through, for example, the electron-transport chain (Grishanin et al, 1997 ). Redoxsensing proteins such as FixL and ArcA (de Philip et al, 1990;Iuchi et al, 1990) are well characterized in bacteria.…”

Metabolism is required for chemotaxis to sugars in Rhodobacter sphaeroides

“…It is also possible that the chemotactic signal results from changes in the redox state of a component of the electron-transport chain, with NADH providing the link between sugar metabolism and electron transport, particularly as mannitol elicits such a strong response and requires a dehydrogenase as the first metabolic step. Redox sensors such as the PrrA/PrrB two-component system, which is involved in the oxygen control of photosynthesis gene expression, are well characterized in R. sphaeroides (Eraso & Kaplan, 1994, 1995 and recent work in this laboratory has shown that redox sensing is involved in tactic responses to light and oxygen (Grishanin et al, 1997). Current work is focused on the identification of the 'sensor' which may link metabolism and electron transport.…”

Analysis of a chemotaxis operon from Rhodospirillum centenum

“…These results have led to the current dogma that the scotophobic response is mediated by the perception of a sudden decrease in the rate of photosynthesis rather than by light absorption through a specific photoreceptor. The mechanism of measuring a reduction in the efficiency of photosynthesis appears to involve monitoring alterations in the rate of photosynthesis-driven electron transport (10,14).The use of the bacterium Rhodospirillum centenum as a model organism for studying bacterial photoperception is particularly appealing since it is known to exhibit two distinctive photosensory processes (29,30). When grown in liquid medium, R. centenum cells, which are motile by means of a single polar flagellum, exhibit a typical scotophobic response.…”

“…These results have led to the current dogma that the scotophobic response is mediated by the perception of a sudden decrease in the rate of photosynthesis rather than by light absorption through a specific photoreceptor. The mechanism of measuring a reduction in the efficiency of photosynthesis appears to involve monitoring alterations in the rate of photosynthesis-driven electron transport (10,14).…”