Cross-Modulation of Homeostatic Responses to Temperature, Oxygen and Carbon Dioxide inC. elegans

Autor: Mario de Bono, Einav Gross, Eiji Kodama-Namba, K. Emanuel Busch, Andrew Jonathan Bretscher, Lorenz A. Fenk
Jazyk: angličtina
Rok vydání: 2013
Předmět:
Zdroj: Kodama-namba, E, Fenk, L A, Bretscher, A J, Gross, E, Busch, K E & De Bono, M 2013, ' Cross-Modulation of Homeostatic Responses to Temperature, Oxygen and Carbon Dioxide inC. elegans ', PLoS Genetics, vol. 9, no. 12, pp. e1004011 . https://doi.org/10.1371/journal.pgen.1004011
PLoS Genetics, Vol 9, Iss 12, p e1004011 (2013)
PLoS Genetics
DOI: 10.1371/journal.pgen.1004011
Popis: Different interoceptive systems must be integrated to ensure that multiple homeostatic insults evoke appropriate behavioral and physiological responses. Little is known about how this is achieved. Using C. elegans, we dissect cross-modulation between systems that monitor temperature, O2 and CO2. CO2 is less aversive to animals acclimated to 15°C than those grown at 22°C. This difference requires the AFD neurons, which respond to both temperature and CO2 changes. CO2 evokes distinct AFD Ca2+ responses in animals acclimated at 15°C or 22°C. Mutants defective in synaptic transmission can reprogram AFD CO2 responses according to temperature experience, suggesting reprogramming occurs cell autonomously. AFD is exquisitely sensitive to CO2. Surprisingly, gradients of 0.01% CO2/second evoke very different Ca2+ responses from gradients of 0.04% CO2/second. Ambient O2 provides further contextual modulation of CO2 avoidance. At 21% O2 tonic signalling from the O2-sensing neuron URX inhibits CO2 avoidance. This inhibition can be graded according to O2 levels. In a natural wild isolate, a switch from 21% to 19% O2 is sufficient to convert CO2 from a neutral to an aversive cue. This sharp tuning is conferred partly by the neuroglobin GLB-5. The modulatory effects of O2 on CO2 avoidance involve the RIA interneurons, which are post-synaptic to URX and exhibit CO2-evoked Ca2+ responses. Ambient O2 and acclimation temperature act combinatorially to modulate CO2 responsiveness. Our work highlights the integrated architecture of homeostatic responses in C. elegans.
Author Summary Many animals are either attracted or repelled by carbon dioxide. We show that the way C. elegans responds to CO2 depends on the temperature it has acclimated to and the oxygen tensions it is experiencing. The effects of acclimation temperature are mediated by a temperature-sensing neuron called AFD that also responds to CO2. The responses evoked in AFD by a change in CO2 concentration are reprogrammed by acclimation temperature. This reprogramming does not appear to require synaptic input from other neurons. O2 modulates CO2 avoidance by setting the activity of the tonically signalling O2 sensor URX. A switch from 21% to 19% O2 is sufficient to convert CO2 from a neutral stimulus to an aversive one in a C. elegans wild strain. Modulation of CO2 responses by O2 cues requires the interneuron RIA which itself responds to changes in CO2 and is directly post-synaptic to URX. CO2 gradients are likely to be common in rotting fruit where Caenorhabditis live. Such gradients could be associated with food, pathogens, conspecifics or predators of C. elegans. The value of CO2 as a sensory cue thus depends crucially on context. This may explain the remarkable complexity of CO2 sensing in C. elegans.
Databáze: OpenAIRE
Externí odkaz: