Key Concepts:

Figure 1. A model for photosensory and chemosensory signalling pathways in Rhodobacter sphaeroides. Photoactive yellow protein (PYP) elicits repellent responses via an as yet unknown pathway (indicated by the question mark) that probably involves a CheA-like histidine kinase and a CheY-like reponse regulator. Attractant responses to light are elicited by increases in the rate of photosynthetic electron transport (blue arrows), which is coupled to proton pumping (brown arrow) across the photosynthetic membranes. The rate of electron transport may be sensed via the FAD prosthetic group of an Aer-related methyl-accepting chemotaxis protein (MCP_Aer), which in turn passes attractant signals to CheW_II, CheA_II and thence to a CheY-related protein. Chemotactic attractant signals are passed via multiple CheW, -A and -Y proteins to converge with the signalling pathways for phototaxis. Genes involved in chemosensory and photosensory signal transduction are found in multiple loci, as shown in the inset. All are transcribed from left to right and some are transcribed as parts of large polycistronic transcripts from the operons shown. Red arrows indicate repellent signals, and green arrows indicate attractant signals. Attractant signals inhibit, whereas repellent signals enhance, the rate of phosphorylation of CheY. Interaction of the phosphorylated form of CheY with the flagellar motor switch causes the motor in Rba. sphaeroides to cease rotation.

Figure 2. A model for photosensory signalling pathways in Halobacterium salinarum. Interconversions between the different forms of the two photoreceptors SRI and SRII are indicated by black arrows, and the yellow hv labels indicate which steps are light-driven. SRI can exist in both attractant (S₃₇₃) and repellent (S^b₅₁₀) signalling states and S₃₇₃ is converted back to SRI₅₈₇, either via S^b₅₁₀ in a fast light-dependent pathway or via a slower light-independent route. The signalling state(s) of SR_II pass repellent signals to the flagellar motors. Attractant signals (green arrows) inhibit, and repellent signals (red arrows) enhance, the rate of phosphorylation of CheY. Interaction of the phosphorylated form of CheY with the flagellar motor switch causes reversal of the direction of motor rotation.

Figure 3. A model for Dictyostelium slug photosensory and thermosensory signalling pathways. The top panel shows a pseudocolour image of two slugs migrating on a water agar surface towards a light source to the right of the figure. Each slug is about a millimetre in length and migrates across the agar surface at about 1 mm h^–1. The lower panel shows a lateral view of a migrating slug. The ‘thought bubbles’ emanating from the tip indicate that the tip controls slug behaviour via the indicated pathways. Signals from photoreceptor and thermoreceptor converge early and thence control the concentrations of the intracellular second messengers cAMP, cGMP, Ca²⁺ and possibly IP₃. The evidence for inositol polyphosphate (IP₃) involvement is the pharmacological effect of Li⁺, whose target could also (or instead) be glycogen synthase kinase 3 (GSK3). Heterotrimeric (G1, G4, G7 and G8) and small (RasD) GTP-binding proteins and their regulators (MEGAP1 or WAVE-associated RacGAP Protein (WRP), RasGEFE and RasGEFL) are involved in transducing the signals to regulate components of the actomyosin cytoskeleton. At least some of the signalling proteins (RasD, Erk2, PKB and GRP125) are recruited by the actin-binding scaffolding protein filamin into a photosensory signalling complex. This modulates the tip activation and inhibition signals that determine the position of the slug tip. Transient lateral imbalances between tip activation and inhibition thus induced by light and temperature gradients cause temporary lateral shifts in tip position and thence slug turning, because the slug ‘follows its nose’. Depending upon whether tip activation or inhibition dominates the response, the slug turns either towards or away from the light source, or up or down the temperature gradient. Sign reversals in slug turning responses result from switches in the balance between control by tip activation and inhibition. This explains direction-dependent sign reversals in phototaxis that cause bidirectional phototaxis and temperature-dependent sign reversals in thermotaxis that cause movement towards the warmth or the cold depending on the temperature. Tip activation signals are believed to be carried by three-dimensional spiral scroll waves of extracellular cAMP (shown in cyan in the lower panel, with the direction of propagation in red) analogous to the two-dimensional cAMP waves that mediate aggregation. At the rear boundary of the tip region, the wave twists and breaks into a train of planar waves that propagate backwards through the rear of the slug. Candidate tip inhibitors are slug turning factor (STF), ammonia and adenosine. Some of the elements used in this figure were kindly provided by Dr Siegert F, Ludwig Maximilians University, Munich, Germany.