Molecular and sensory basis of a food related two-state behavior in C. elegans

Abstract

Most animals display multiple behavioral states and control the time allocation to each of their activity phases depending on their environment. Here we develop a new quantitative method to analyze Caenorhabditis elegans behavioral states. We show that the dwelling and roaming two-state behavior of C. elegans is tightly controlled by the concentration of food in the environment of the animal. Sensory perception through the amphid neurons is necessary to extend roaming phases while internal metabolic perception of food nutritional value is needed to induce dwelling. Our analysis also shows that the proportion of time spent in each state is modulated by past nutritional experiences of the animal. This two-state behavior is regulated through serotonin as well as insulin and TGF-beta signaling pathways. We propose a model where food nutritional value is assessed through internal metabolic signaling. Biogenic amines signaling could allow the worm to adapt to fast changes in the environment when peptide transcriptional pathways may mediate slower adaptive changes.

Figure 1. Two-state behavior of wild type C. elegans on food.

(A) Trajectories of multiple WT C. elegans on OP50 (60 mm plate) (B) Curvature histogram for all the wild type worms (1bin = 1°) (C) Speed histogram for all the wild type worms (1bin = 0.05 mm/s) (D) Data points density map in the (Speed, curvature) plane. Two clusters can be observed (Data from 38 worms) (E) Clustering method. Data points over line A are attributed to the roaming phase, data points under line A to the dwelling phase. Line A has been determined on total WT data and is used for analysis of all the experiments in all the conditions.

Figure 2. C. elegans adapts its roaming behavior to food concentration, both by changing the dwelling/roaming percentage and the speed during the roaming phase.

(A–D) Speed histograms of WT C. elegans on different concentration of bacteria (A: 5 10⁴ B: 1.5 10⁵ C: 3 10⁵ D: 5 10⁵ bacteria per cm², at least 15 worms have been recorded per condition, results are presented as mean ± s.e.m.) (E) Speed in the roaming phase decreases with food concentration (F) The percentage of time spent in the roaming phase is a function of food concentration (logarithm scale). Worms switch from an all-roaming to mostly dwelling in one decade of food concentration.

Figure 3. Influence of food perception and experience.

(A–B) Data density maps for (A) N2 worms feeding on aztreonam treated bacteria. Compared to N2 worms in standard conditions (Fig 1-D) the dwelling cluster is suppressed (B) N2 worms feeding on standard OP50 bacteria after a 1 h fasting period. The roaming cluster is suppressed. Insert: Proportion of time spent roaming during the 0–20 min, 20–40 min and 40–60 min time intervals after a one-hour starvation period. (C) Quantitative measurements of the percentage of time spent roaming of N2 worms in aztreonam (A) and fasting (B) conditions and of mutants that have sensory perception defects. At least 20 worms were recorded per condition. Results are presented as mean ± s.e.m. *Different from wild type, p<0.01 **Different from each other p<0.01.

Figure 4. Biogenic amines, insulin and TGF-beta signaling mutants.

(A) Percentage of time spent roaming for well-fed and fasted biogenic amines mutants in standard conditions. (B) Percentage of time spent roaming for well-fed and fasted insulin and TGF beta signaling mutants in standard conditions and on aztreonam-treated OP50. At least 20 worms were recorded per condition. Results are presented as mean ± s.e.m. *Different from wild type, Student's t-test p<0.01. ***Different from wild type p<0.05. **Different from each other p<0.01. ^#Different from wild type on atreonam treated bacteria p<0.01.

Figure 5. Proposed schematic representation of the control of the dwelling and roaming behavior by sensory perception and internal signaling.