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

   https://doi.org/10.7554/eLife.56186  

   Schiffer, Jodie A; Servello, Francesco A; Heath, William R; Amrit, Francis Raj; Stumbur, Stephanie V; Eder, Matthias; Martin, Olivier MF; Johnsen, Sean B; Stanley, Julian A; Tam, Hannah; et al (May 2020, eLife)

   null (Ed.)

   Cells of all kinds often wage chemical warfare against each other. Hydrogen peroxide is often the weapon of choice on the microscopic battlefield, where it is used to incapacitate opponents or to defend against attackers. For example, some plants produce hydrogen peroxide in response to infection to fight off disease-causing microbes. Individual cells have also evolved defenses to prevent or repair ‘injuries’ caused by hydrogen peroxide. These are similar across many different species. They include enzymes called catalases, which break down hydrogen peroxide, and others to repair damage. However, scientists still do not fully understand how animals and other multicellular organisms might coordinate these defenses across their cells. Caenorhabditis elegans is a microscopic species of worm that lives in rotting fruits. It often encounters the threat of cellular warfare: many types of bacteria in its environment generate hydrogen peroxide, and some can make enough to kill the worms outright. Like other organisms, C. elegans also produces catalases to defend itself against hydrogen peroxide attacks. However, it must activate its defenses at the right time; if it did so when they were not needed, this would result in a detrimental energy ‘cost’ to the worm. Although C. elegans is a small organism containing only a defined number of cells, exactly why and how it switches its chemical defenses on or off remains unknown. Schiffer et al. therefore set out to determine how C. elegans controls these defenses, focusing on the role of the brain in detecting and processing information from its environment. Experiments looking at the brains of genetically manipulated worms revealed a circuit of sensory nerve cells whose job is to tell the rest of the worm’s tissues that they no longer need to produce defense enzymes. Crucially, the circuit became active when the worms sensed E. coli bacteria nearby. Bacteria in the same family as E. coli are normally found in in the same habitat as C. elegans and these bacteria are also known to make enzymes of their own to eliminate hydrogen peroxide around them. These results indicate that C. elegans can effectively decide, based on the activity of its circuit, when to use its own defenses and when to ‘freeload’ off those of neighboring bacteria. This work is an important step towards understanding how sensory circuits in the brain can control hydrogen peroxide defenses in multicellular organisms. In the future, it could help researchers work out how more complex animals, like humans, coordinate their cellular defenses, and therefore potentially yield new strategies for improving health and longevity. 

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

   https://doi.org/10.1371/journal.ppat.1010112  

   Schiffer, Jodie A.; Stumbur, Stephanie V.; Seyedolmohadesin, Maedeh; Xu, Yuyan; Serkin, William T.; McGowan, Natalie G.; Banjo, Oluwatosin; Torkashvand, Mahdi; Lin, Albert; Hosea, Ciara N.; et al (December 2021, PLOS Pathogens)

   Weaver, Benjamin (Ed.)

   Hydrogen peroxide (H 2 O 2 ) is the most common chemical threat that organisms face. Here, we show that H 2 O 2 alters the bacterial food preference of Caenorhabditis elegans , enabling the nematodes to find a safe environment with food. H 2 O 2 induces the nematodes to leave food patches of laboratory and microbiome bacteria when those bacterial communities have insufficient H 2 O 2 -degrading capacity. The nematode’s behavior is directed by H 2 O 2 -sensing neurons that promote escape from H 2 O 2 and by bacteria-sensing neurons that promote attraction to bacteria. However, the input for H 2 O 2 -sensing neurons is removed by bacterial H 2 O 2 -degrading enzymes and the bacteria-sensing neurons’ perception of bacteria is prevented by H 2 O 2 . The resulting cross-attenuation provides a general mechanism that ensures the nematode’s behavior is faithful to the lethal threat of hydrogen peroxide, increasing the nematode’s chances of finding a niche that provides both food and protection from hydrogen peroxide. 

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3. A neurotransmitter produced by gut bacteria modulates host sensory behavior.

   https://doi.org/DOI: 10.1038/s41586-020-2395-5  

   O'Donnell, Michael P; Fox, Bennett W; Chao, Pin-Hao; Schroeder, Frank C; Sengupta, Piali (June 2020, Nature)

   Animals coexist in commensal, pathogenic or mutualistic relationships with complex communities of diverse organisms, including microorganisms1. Some bacteria produce bioactive neurotransmitters that have previously been proposed to modulate nervous system activity and behaviours of their hosts2,3. However, the mechanistic basis of this microbiota-brain signalling and its physiological relevance are largely unknown. Here we show that in Caenorhabditis elegans, the neuromodulator tyramine produced by commensal Providencia bacteria, which colonize the gut, bypasses the requirement for host tyramine biosynthesis and manipulates a host sensory decision. Bacterially produced tyramine is probably converted to octopamine by the host tyramine β-hydroxylase enzyme. Octopamine, in turn, targets the OCTR-1 octopamine receptor on ASH nociceptive neurons to modulate an aversive olfactory response. We identify the genes that are required for tyramine biosynthesis in Providencia, and show that these genes are necessary for the modulation of host behaviour. We further find that C. elegans colonized by Providencia preferentially select these bacteria in food choice assays, and that this selection bias requires bacterially produced tyramine and host octopamine signalling. Our results demonstrate that a neurotransmitter produced by gut bacteria mimics the functions of the cognate host molecule to override host control of a sensory decision, and thereby promotes fitness of both the host and the microorganism. 

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4. Persistent thermal input controls steering behavior in Caenorhabditis elegans

   https://doi.org/10.1371/journal.pcbi.1007916  

   Ikeda, Muneki; Matsumoto, Hirotaka; Izquierdo, Eduardo J. (January 2021, PLOS Computational Biology)

   Ahamed, Tosif (Ed.)

   Motile organisms actively detect environmental signals and migrate to a preferable environment. Especially, small animals convert subtle spatial difference in sensory input into orientation behavioral output for directly steering toward a destination, but the neural mechanisms underlying steering behavior remain elusive. Here, we analyze a C . elegans thermotactic behavior in which a small number of neurons are shown to mediate steering toward a destination temperature. We construct a neuroanatomical model and use an evolutionary algorithm to find configurations of the model that reproduce empirical thermotactic behavior. We find that, in all the evolved models, steering curvature are modulated by temporally persistent thermal signals sensed beyond the time scale of sinusoidal locomotion of C . elegans . Persistent rise in temperature decreases steering curvature resulting in straight movement of model worms, whereas fall in temperature increases curvature resulting in crooked movement. This relation between temperature change and steering curvature reproduces the empirical thermotactic migration up thermal gradients and steering bias toward higher temperature. Further, spectrum decomposition of neural activities in model worms show that thermal signals are transmitted from a sensory neuron to motor neurons on the longer time scale than sinusoidal locomotion of C . elegans . Our results suggest that employments of temporally persistent sensory signals enable small animals to steer toward a destination in natural environment with variable, noisy, and subtle cues. 

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5. C. elegans enteric motor neurons fire synchronized action potentials underlying the defecation motor program

   https://doi.org/10.1038/s41467-022-30452-y  

   Jiang, Jingyuan; Su, Yifan; Zhang, Ruilin; Li, Haiwen; Tao, Louis; Liu, Qiang (May 2022, Nature Communications)

   Abstract C. elegansneurons were thought to be non-spiking until our recent discovery of action potentials in the sensory neuron AWA; however, the extent to which theC. elegansnervous system relies on analog or digital coding is unclear. Here we show that the enteric motor neurons AVL and DVB fire synchronous all-or-none calcium-mediated action potentials following the intestinal pacemaker during the rhythmicC. elegansdefecation behavior. AVL fires unusual compound action potentials with each depolarizing calcium spike mediated by UNC-2 followed by a hyperpolarizing potassium spike mediated by a repolarization-activated potassium channel EXP-2. Simultaneous behavior tracking and imaging in free-moving animals suggest that action potentials initiated in AVL propagate along its axon to activate precisely timed DVB action potentials through the INX-1 gap junction. This work identifies a novel circuit of spiking neurons inC. elegansthat uses digital coding for long-distance communication and temporal synchronization underlying reliable behavioral rhythm. 

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