The yellow lines are isothermal tracks in a horizontal temperature gradient.
People who grew up in California tend to prefer warm weather and must learn the art of layering warm clothing when moving to colder climates. Like humans, other animals also learn and adapt to the temperature of their environment. Biron et al. report that diacylglycerol kinase modulates the rate of adaptation to new temperatures in C. elegans in a recent article in Nature Neuroscience.
C. elegans learn the temperatures of environments they have been in for even short lengths of time. In a thermal gradient, they 'track' isotherms, which are temperatures similar to the ones they know. When they reach their learned temperature, they move in straight paths perpendicular to the gradient. This learned temperature is called the thermotactic set-point. The authors plotted the thermotactic set-point over time in C. elegans shifted to warmer or colder temperatures and found that the resetting of the thermotactic set-point formed an exponential function.
The gene encoding diacylglycerol (DAG) kinase (DGK), dgk-3, is enriched in AFD neurons, which are necessary for thermosensory behaviors. The authors generated dgk-3 knockout worms. Dgk-3 knockouts that were incubated overnight at 15°C and transfered to 25°C initially showed a lower thermotactic set-point relative to wild-type worms. Over time, dgk-3 knockouts shifted their thermotactic set-points more slowly than wild-type worms. dgk-3 knockouts that were transferred from 25°C to 15°C also initially showed a lower thermotactic set-point than did wild-type worms. However, set-point shifts were slightly faster in dgk-3 knockout relative to wild-type worms.
DGK reduces the concentration of the second messenger DAG by converting it to phosphatidic acid. DGKs have motifs that bind calcium and restrain DGK activity. The authors deleted the calcium-binding motifs from DGK-3 to generate C. elegans with overactive DGK-3. In contrast to dgk-3 knockouts, these worms reset from 15°C to 25°C slightly faster and reset from 25°C to 15°C slower than wild-type worms. Conversely, wild-type worms treated with the DAG analog TPA were similar to dgk-3 knockouts, with lower thermotactic set-points relative to untreated worms, suggesting that increased concentrations of DAG slow the resetting of thermal memory in C. elegans.
Calcium signaling in AFD neurons is involved in thermosensory memory and is sensitive to changes in temperature. Above a temperature called T*, oscillations in temperature produce identical oscillations in intracellular calcium concentration. Like the thermotactic set-point, T* is set by environmental temperature and shifts exponentially over time. T* in AFD neurons was not affected by dgk-3 deficiency. However, T* in AIY neurons, which receive input from AFD neurons, was affected. When the authors shifted worms to higher temperatures, the T* in AIY neurons reset more slowly in dgk-3 knockout relative to wild-type worms, suggesting that DGK-3 affects the synaptic output of AFD neurons.
The authors speculate that in AFD neurons, elevated concentrations of DAG decrease the threshold for synaptic output to AIY neurons, resulting in the tracking of lower temperatures. DAG and its regulator DGK are therefore important in learning and adaptation in C. elegans and should be examined for similar roles in mammals.