Abstract
In a population, chemical communication determines the response of animals to changing environmental conditions, what leads to an enhanced resistance against stressors. In response to starvation, the nematode Caenorhabditis elegans arrest post-embryonic development at the first larval stage (L1) right after hatching. As arrested L1 larvae, C. elegans become more resistant to diverse stresses, allowing them to survive for several weeks expecting to encounter more favorable conditions. L1 arrested at high densities display an enhanced resistance to starvation, dependent on soluble compounds released beyond hatching and the first day of arrest. Here, we show that this chemical communication also influences recovery after prolonged periods in L1 arrest. Animals at high density recovered faster than animals at low density. We found that the density effect on survival depends on the final effector of the insulin signaling pathway, the transcription factor DAF-16. Moreover, DAF-16 activation was higher at high density, consistent with a lower expression of the insulin-like peptide DAF-28 in the neurons. The improved recovery of animals after arrest at high density depended on soluble compounds present in the media of arrested L1s. In an effort to find the nature of these compounds, we investigated the disaccharide trehalose as putative signaling molecule, since its production is enhanced during L1 arrest and it is able to activate DAF-16. We detected the presence of trehalose in the medium of arrested L1 larvae at a low concentration. The addition of this concentration of trehalose to animals arrested at low density was enough to rescue DAF-28 production and DAF-16 activation to the levels of animals arrested at high density. However, despite activating DAF-16, trehalose was not capable of reversing survival and recovery phenotypes, suggesting the participation of additional signaling molecules. With all, here we describe a molecular mechanism underlying social communication that allows C. elegans to maintain arrested L1 larvae ready to quickly recover as soon as they encounter nutrient sources.
Highlights
Animals arrested at high density present a lower insulin signaling that results in a higher activation of DAF-16, which is responsible for the enhanced recovery capacity after starvation
We recently showed that recovery time after extended arrest is regulated by insulin/IGF-1-like signaling (IIS) in a DAF16 dependent manner, being shorter in a daf-2 mutant and longer in a daf-16 mutant strain (Olmedo et al, 2020)
We found a higher DAF-28 production in L1 larvae at low density after 1 day of arrest, which correlates with a lower activation of DAF-16 at this density
Summary
Chemical communication between individuals of the same population determines the social behavior in response to environmental variations in a wide variety of species, from bacteria to mammals (Taga and Bassler, 2003; Benabentos et al, 2009; Sokolowski, 2010; Coombes et al, 2018; Doyle and Meeks, 2018; Mukherjee and Bassler, 2019; Brückner and Parker, 2020; Yan et al, 2020). Larvae arrested at high densities display an enhanced resistance to starvation This effect of larval density on survival depends on chemical communication between animals, in which the participation of sensory neurons is required. Animals arrested at high density present a lower insulin signaling that results in a higher activation of DAF-16, which is responsible for the enhanced recovery capacity after starvation. In an attempt to find communication molecules mediating the density effect, we investigated trehalose as a putative signal initiating the response This disaccharide is present in the medium of arrested L1s at a low, density-dependent concentration. Trehalose supplementation is not sufficient to reverse the shorter lifespan and longer recovery time of animals starved at low density, indicating that additional communication molecules are needed to completely explain the density effect on arrested L1 larvae, and that DAF-16 is necessary but not sufficient to regulate such effect
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