Dataset Information

Identification of Odor Blend Used by Caenorhabditis elegans for Pathogen Recognition.

ABSTRACT: Animals have evolved specialized pathways to detect appropriate food sources and avoid harmful ones. Caenorhabditis elegans can distinguish among the odors of various species of bacteria, its major food source, but little is known about what specific chemical cue or combination of chemical cues C. elegans uses to detect and recognize different microbes. Here, we examine the strong innate attraction of C. elegans for the odor of the pathogenic bacterium, Serratia marcescens. This initial attraction likely facilitates ingestion and infection of the C. elegans host. Using solid-phase microextraction and gas chromatography coupled with mass spectrometry, we identify 5 volatile odors released by S. marcescens and identify those that are attractive to C. elegans. We use genetic methods to show that the amphid chemosensory neuron, AWCON, senses both S. marcescens-released 2-butanone and acetone and drives attraction to S. marcescens. In C. elegans, pairing a single odorant with food deprivation results in a reduced attractive response for that specific odor. We find that pairing the natural odor of S. marcescens with food deprivation results in a reduced attraction for the natural odor of S. marcescens and a similar reduced attraction for the synthetic blend of acetone and 2-butanone. This result indicates that only 2 odorants represent the more complex odor bouquet of S. marcescens. Although bacterial-released volatiles have long been known to be attractive to C. elegans, this study defines for the first time specific volatile cues that represent a particular bacterium to C. elegans.

SUBMITTER: Worthy SE

PROVIDER: S-EPMC6018680 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Identification of Odor Blend Used by Caenorhabditis elegans for Pathogen Recognition.

Worthy Soleil E SE Rojas German L GL Taylor Charles J CJ Glater Elizabeth E EE

Chemical senses 20180201 3

Animals have evolved specialized pathways to detect appropriate food sources and avoid harmful ones. Caenorhabditis elegans can distinguish among the odors of various species of bacteria, its major food source, but little is known about what specific chemical cue or combination of chemical cues C. elegans uses to detect and recognize different microbes. Here, we examine the strong innate attraction of C. elegans for the odor of the pathogenic bacterium, Serratia marcescens. This initial attracti ...[more]

PMID: 29373666

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Project description:We developed a mathematical model of a hypothetical neuronal signal transduction pathway to better understand olfactory perception in Caenorhabditis elegans. This worm has only three pairs of olfactory receptor neurons. Intracellular Ca(2+) decreases in one pair of olfactory neurons in C. elegans, the AWC neurons, following application of an attractive odor and there is a transient increase in intracellular Ca(2+) following removal of odor. The magnitude of this increase is positively correlated with the duration of odor stimulation. Additionally, this Ca(2+) transient is induced by a cGMP second messenger system. We identified likely candidates for the signal transduction molecules functioning in this system based on available gene expression and physiological data from AWCs. Our model incorporated a G-protein-coupled odor receptor, a G-protein, a guanylate cyclase as the G-protein effector, and a single phosphodiesterase. Additionally, a cyclic-nucleotide-gated ion channel and a voltage-gated ion channel that mediated calcium influx were incorporated into the model. We posited that, upon odor stimulation, guanylate cyclase was suppressed by the G-protein and that, upon cessation of the stimulus, the G-protein-induced suppression ceased and cGMP synthesis was restored. A key element of our model was a Ca(2+)-dependent negative feedback loop that ensured that the calcium increases were transient. Two guanylate cyclase-activating proteins acted on the effector guanylate cyclase to negatively regulate cGMP signaling and the resulting calcium influx. Our model was able to closely replicate in silico three important features of the calcium dynamics of AWCs. Specifically, in our simulations, [Ca(2+)] increased rapidly and reached its peak within 10 s after the odor stimulus was removed, peak [Ca(2+)] increased with longer odor exposure, and [Ca(2+)] decreased during a second stimulus that closely followed an initial stimulus. However, application of random background signal ('noise') showed that certain components of the pathway were particularly sensitive to this noise.

Project description:BackgroundAn essential stage of neural development involves the assembly of neural circuits via formation of inter-neuronal connections. Early steps in neural circuit formation, including cell migration, axon guidance, and the localization of synaptic components, are well described. However, upon reaching their target region, most neurites still contact many potential partners. In order to assemble functional circuits, it is critical that within this group of cells, neurons identify and form connections only with their appropriate partners, a process we call synaptic partner recognition (SPR). To understand how SPR is mediated, we previously developed a genetically encoded fluorescent trans-synaptic marker called NLG-1 GRASP, which labels synaptic contacts between individual neurons of interest in dense cellular environments in the genetic model organism Caenorhabditis elegans.ResultsHere, we describe the first use of NLG-1 GRASP technology, to identify SPR genes that function in this critical process. The NLG-1 GRASP system allows us to assess synaptogenesis between PHB sensory neurons and AVA interneurons instantly in live animals, making genetic analysis feasible. Additionally, we employ a behavioral assay to specifically test PHB sensory circuit function. Utilizing this approach, we reveal a new role for the secreted UNC-6/Netrin ligand and its transmembrane receptor UNC-40/Deleted in colorectal cancer (DCC) in SPR. Synapses between PHB and AVA are severely reduced in unc-6 and unc-40 animals despite normal axon guidance and subcellular localization of synaptic components. Additionally, behavioral defects indicate a complete disruption of PHB circuit function in unc-40 mutants. Our data indicate that UNC-40 and UNC-6 function in PHB and AVA, respectively, to specify SPR. Strikingly, overexpression of UNC-6 in postsynaptic neurons is sufficient to promote increased PHB-AVA synaptogenesis and to potentiate the behavioral response beyond wild-type levels. Furthermore, an artificially membrane-tethered UNC-6 expressed in the postsynaptic neurons promotes SPR, consistent with a short-range signal between adjacent synaptic partners.ConclusionsThese results indicate that the conserved UNC-6/Netrin-UNC-40/DCC ligand-receptor pair has a previously unknown function, acting in a juxtacrine manner to specify recognition of individual postsynaptic neurons. Furthermore, they illustrate the potential of this new approach, combining NLG-1 GRASP and behavioral analysis, in gene discovery and characterization.

Dataset Information

Identification of Odor Blend Used by Caenorhabditis elegans for Pathogen Recognition.

Publications

Identification of Odor Blend Used by Caenorhabditis elegans for Pathogen Recognition.

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