Abstract
Chemosensation is indispensable for the survival of Caenorhabditis elegans to discriminate food and pathogenic bacteria in their living environment. Food-like odors emitted by the pathogen Bacillus nematocida B16 for trapping its hosts and an olfactory signaling pathway responsible to sense the attractant 2-heptanone were identified in our previous study. Here, we further explore how the worms recognize the attractive molecules indole and 2-ethyl hexanol, which have different chemical properties and modest nematode-luring ability. We show that the chemotaxis toward indole and 2-ethyl hexanol requires the G protein-coupled receptors encoded by str-193 on AWC and str-7 on AWA. In a further genetic screen for downstream effectors in olfactory signaling cascades, the Gα subunit GSA-1, guanylyl cyclase ODR-1 and DAF-11 and the cGMP-gated channel TAX-2/TAX-4 were found to be necessary for indole sensation, whereas the TRPV channels OSM-9/OCR-2 and the PLC pathway activated by GPA-6 are responsible for the detection of 2-ethyl hexanol. Altogether, our current work further clarifies the distinct olfactory signaling pathways through which C. elegans senses different chemicals and is lured by B. nematocida B16, improving our comprehensive understanding of the mechanisms by which bacterial pathogens effectively infect their hosts.
Similar content being viewed by others
References
Böttger, A., Vothknecht, U., Bolle, C., and Wolf, A. (2018). GPCRs. In Lessons on Caffeine, Cannabis & Co, ed. Springer Nature Switzerland AG, pp. 29–42.
Bargmann, C.I. (2006a). Chemosensation in C. elegans. In Wormbook, ed. The C.elegans Research Community, WormBook, https://doi.org/10.1895/wormbook.1.123.1, http://www.wormbook.org.
Bargmann, C.I. (2006b). Comparative chemosensation from receptors to ecology. Nature 444, 295–301.
Bargmann, C.I., Hartwieg, E., and Horvitz, H.R. (1993). Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74, 515–527.
Bastiani, C., and Mendel, J. (2006). Heterotrimeric G proteins in C. elegans. In Wormbook, ed. The C. elegans Research Community, WormBook, https://doi.org/10.1895/wormbook.1.75.1, http://www.wormbook.org.
Bergamasco, C., and Bazzicalupo, P. (2006). Signaling in the chemosensory systems. Cell Mol Life Sci 63, 1510–1522.
Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71–94.
Chou, J., Troemel, E., Sengupta, P., Colbert, H., Tong, L., Tobin, D., Roayaie, K., Crump, J., Dwyer, N., and Bargmann, C.I. (1996). Olfactory recognition and discrimination in Caenorhabditis elegans. Cold Spring Harb Symp Quantitat Biol 61, 157–164.
Coburn, C.M., and Bargmann, C.I. (1996). A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695–706.
Colbert, H.A., and Bargmann, C.I. (1995). Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14, 803–812.
Duc, N.M., Kim, H.R., and Chung, K.Y. (2015). Structural mechanism of G protein activation by G protein-coupled receptor. Eur J Pharmacol 763, 214–222.
Ezak, M.J., and Ferkey, D.M. (2011). A functional nuclear localization sequence in the C. elegans TRPV channel OCR-2. PLoS ONE 6, e25047.
Gaillard, I., Rouquier, S., and Giorgi, D. (2004). Olfactory receptors. Cell Mol Life Sci 61, 456–469.
Hardie, R.C. (2007). TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol 578, 9–24.
Hukema, R.K. (2006). Gustatory behaviour in Caenorhabditis elegans. MGC Department of Cell Biology and Genetics. Erasmus MC, Rotterdam, The Netherlands, 176.
Kamath, R.S., Fraser, A.G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M., et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231–237.
Kariya, K.I., Bui, Y.K., Gao, X., Sternberg, P.W., and Kataoka, T. (2004). Phospholipase c regulates ovulation in Caenorhabditis elegans. Dev Biol 274, 201–210.
Komatsu, H., Jin, Y.H., L’Etoile, N., Mori, I., Bargmann, C.I., Akaike, N., and Ohshima, Y. (1999). Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res 821, 160–168.
Lans, W.J. (2005). Making sense of G proteins: Genetic analysis of sensory G protein signaling in the nematode C. elegans. Dissertation for Doctoral Degree. (Erasmus MC: University Medical Center Rotterdam).
Lee, J.H., Wood, T.K., and Lee, J. (2015). Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23, 707–718.
L’Etoile, N.D., and Bargmann, C.I. (2000). Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase odr-1. Neuron 25, 575–5
Liu, J., Ward, A., Gao, J., Dong, Y., Nishio, N., Inada, H., Kang, L., Yu, Y., Ma, D., Xu, T., et al. (2010). C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat Neurosci 13, 715–722.
Margie, O., Palmer, C., and Chin-Sang, I. (2013)C. elegans Chemotaxis Assay. JoVE.
Mariol, M.C., Walter, L., Bellemin, S., and Gieseler, K. (2013)A Rapid Protocol for Integrating Extrachromosomal Arrays With High Transmission Rate into the C. elegans Genome. JoVE.
Niu, Q., Huang, X., Zhang, L., Xu, J., Yang, D., Wei, K., Niu, X., An, Z., Wennstrom Bennett, J., Zou, C., et al. (2010). A trojan horse mechanism of bacterial pathogenesis against nematodes. Proc Natl Acad Sci USA 107, 16631–16636.
Pierce, K.L., Premont, R.T., and Lefkowitz, R.J. (2002). Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3, 639–650.
Roayaie, K., Crump, J.G., Sagasti, A., and Bargmann, C.I. (1998). The Gα protein odr-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20, 55–67.
Robertson, H.M., and Thomas, J.H. (2006). The putative chemoreceptor families of C. elegans. In Wormbook, ed. The C. elegans Research Community, WormBook, https://doi.org/10.1895/wormbook.1.66.1, http://www.wormbook.org.
Sengupta, P., Colbert, H.A., and Bargmann, C.I. (1994). The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79, 971–980.
Sengupta, P., Chou, J.H., and Bargmann, C.I. (1996). Odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899–909.
Serizawa, S., Miyamichi, K., and Sakano, H. (2004). One neuron-one receptor rule in the mouse olfactory system. Trends Genet 20, 648–653.
Shidara, H., Hotta, K., and Oka, K. (2017). Compartmentalized cGMP responses of olfactory sensory neurons in Caenorhabditis elegans. J Neurosci 37, 3753–3763.
Spehr, M., and Leinders-Zufall, T. (2005). One neuron-multiple receptors: Increased complexity in olfactory coding? Science’s STKE 285, pe25–pe25.
Stewart, M.K., Clark, N.L., Merrihew, G., Galloway, E.M., and Thomas, J. H. (2005). High genetic diversity in the chemoreceptor superfamily of Caenorhabditis elegans. Genetics 169, 1985–1996.
Suh, B.C., and Hille, B. (2008). PIP2 is a necessary cofactor for ion channel function: How and why? Annu Rev Biophys 37, 175–195.
Timmons, L., Court, D.L., and Fire, A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103–112.
Troemel, E.R., Kimmel, B.E., and Bargmann, C.I. (1997). Reprogramming chemotaxis responses: Sensory neurons define olfactory preferences in C. elegans. Cell 91, 161–169.
Zhang, C., Yan, J., Chen, Y., Chen, C., Zhang, K., and Huang, X. (2014). The olfactory signal transduction for attractive odorants in Caenorhabditis elegans. Biotech Adv 32, 290–295.
Zhang, C., Zhao, N., Chen, Y., Zhang, D., Yan, J., Zou, W., Zhang, K., and Huang, X. (2016). The signaling pathway of Caenorhabditis elegans mediates chemotaxis response to the attractant 2-heptanone in a Trojan horse-like pathogenesis. J Biol Chem 291, 23618–23627.
Zhang, Y., Lu, H., and Bargmann, C.I. (2005). Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438, 179–184.
Zhang, Y., Chou, J.H., Bradley, J., Bargmann, C.I., and Zinn, K. (1997). The Caenorhabditis elegans seven-transmembrane protein odr-10 functions as an odorant receptor in mammalian cells. Proc Natl Acad Sci USA 94, 12162–12167.
Zhu, M., Xu, X.’., Li, Y., Wang, P., Niu, S., Zhang, K., and Huang, X. (2019). Biosynthesis of the nematode attractant 2-heptanone and its co-evolution between the pathogenic bacterium bacillus nematocida and non-pathogenic bacterium Bacillus subtilis. Front Microbiol 10, 1489.
Acknowledgements
This work was supported by the Department of Science and Technology of Yunnan Province (2019FA046) and the National Natural Science Foundation of China (32060632 and 31370162).
Author information
Authors and Affiliations
Corresponding author
Additional information
Compliance and ethics
The author(s) declare that they have no conflict of interest.
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Zhu, M., Chen, Y., Zhao, N. et al. Multiple olfactory pathways contribute to the lure process of Caenorhabditis elegans by pathogenic bacteria. Sci. China Life Sci. 64, 1346–1354 (2021). https://doi.org/10.1007/s11427-020-1842-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-020-1842-7