Caenorhabditis elegans processes sensory information to choose between freeloading and self-defense strategies

Abstract

Hydrogen peroxide is the preeminent chemical weapon that organisms use for combat. Individual cells rely on conserved defenses to prevent and repair peroxide-induced damage, but whether similar defenses might be coordinated across cells in animals remains poorly understood. Here, we identify a neuronal circuit in the nematode Caenorhabditis elegans that processes information perceived by two sensory neurons to control the induction of hydrogen peroxide defenses in the organism. We found that catalases produced by Escherichia coli, the nematode’s food source, can deplete hydrogen peroxide from the local environment and thereby protect the nematodes. In the presence of E. coli, the nematode’s neurons signal via TGFβ-insulin/IGF1 relay to target tissues to repress expression of catalases and other hydrogen peroxide defenses. This adaptive strategy is the first example of a multicellular organism modulating its defenses when it expects to freeload from the protection provided by molecularly orthologous defenses from another species.

Global profiling of distinct cysteine redox forms reveals wide-ranging redox regulation in C. elegans

“…For t-BOOH treatments, OP50-1 was used as food source. For H 2 O 2 treatments, the KatG KatE AhpCF triple null mutant bacterial strain JI377, which cannot scavenge hydrogen peroxide from the environment, was used as the food source 65 .…”

C. elegans: A biosensor for host–microbe interactions

“…Several reports using C. elegans as a model organism published over the last 10 years have provided remarkable insights into host-microbe interactions (Figure 1). For example, several studies using nematode development as a phenotypic readout have shown that its microbiota is essential for the supply of micro-nutrients such as vitamin B2 48 , B6 29 , B9 29,49 , B12 50,51 , iron 21,31,52 and molybdenum 36 , as well as reactive oxygen species 31,53 . The C. elegans model has also proven useful in identifying other metabolites at the interface between microbes and host, which regulate adult physiological traits.…”

“…E. coli screen identifies bacterial folate regulating lifespan (Virk et al 49 ) 137 ) Bacterial small RNAs alter host behaviour (Kaletsky et al 41 )Host-microbe freeloading and self-defense strategies (Schiffer et al53 ) …”

Modulation of sensory perception by hydrogen peroxide enables Caenorhabditis elegans to find a niche that provides both food and protection from hydrogen peroxide

“…To avoid damage from H 2 O 2 , cells rely on conserved physiological defenses, including H 2 O 2 -degrading catalases (Mishra and Imlay, 2012). We recently found that C. elegans represses their own H 2 O 2 defenses in response to sensory perception of Escherichia coli , the nematode’s food source, because E. coli can deplete H 2 O 2 from the local environment and thereby protect the nematodes (Schiffer et al, 2020). Thus, the E. coli self-defense mechanisms create a public good (West et al, 2006), an environment safe from the threat of H 2 O 2 , that benefits C. elegans (Schiffer et al, 2020).…”

“…We recently found that C. elegans represses their own H 2 O 2 defenses in response to sensory perception of Escherichia coli , the nematode’s food source, because E. coli can deplete H 2 O 2 from the local environment and thereby protect the nematodes (Schiffer et al, 2020). Thus, the E. coli self-defense mechanisms create a public good (West et al, 2006), an environment safe from the threat of H 2 O 2 , that benefits C. elegans (Schiffer et al, 2020). Whether similar interactions between nematodes and bacteria shaped the evolution of behavioral responses protecting C. elegans from H 2 O 2 remains poorly understood.…”