title: Caenorhabditis elegans recognizes a bacterial quorum-sensing signal molecule through the AWCON neuron.
abstract: In a process known as quorum sensing, bacteria use chemicals called autoinducers for cell-cell communication. Population-wide detection of autoinducers enables bacteria to orchestrate collective behaviors. In the animal kingdom detection of chemicals is vital for success in locating food, finding hosts, and avoiding predators. This behavior, termed chemotaxis, is especially well studied in the nematode Caenorhabditis elegans. Here we demonstrate that the Vibrio cholerae autoinducer (S)-3-hydroxytridecan-4-one, termed CAI-1, influences chemotaxis in C. elegans. C. elegans prefers V. cholerae that produces CAI-1 over a V. cholerae mutant defective for CAI-1 production. The position of the CAI-1 ketone moiety is the key feature driving CAI-1-directed nematode behavior. CAI-1 is detected by the C. elegans amphid sensory neuron AWC(ON). Laser ablation of the AWC(ON) cell, but not other amphid sensory neurons, abolished chemoattraction to CAI-1. These analyses define the structural features of a bacterial-produced signal and the nematode chemosensory neuron that permit cross-kingdom interaction.
authors.affiliation: Department of Molecular Biology and Princeton University, Princeton, New Jersey 08544.
authors.forename: Kristen M
authors.initials: KM
authors.lastname: Werner
authors.affiliation: Department of Chemistry and Biochemistry, Rowan University, Glassboro, New Jersey 08028.
authors.forename: Lark J
authors.initials: LJ
authors.lastname: Perez
authors.affiliation: Department of Pediatrics-Oncology, Baylor College of Medicine, Houston, Texas 77030, and.
authors.forename: Rajarshi
authors.initials: R
authors.lastname: Ghosh
authors.affiliation: Department of Chemistry, Princeton University, Princeton, New Jersey 08544.
authors.forename: Martin F
authors.initials: MF
authors.lastname: Semmelhack
authors.affiliation: Department of Molecular Biology and Princeton University, Princeton, New Jersey 08544; Howard Hughes Medical Institute, Chevy Chase, Maryland 20815. Electronic address: bbassler@princeton.edu.
authors.forename: Bonnie L
authors.initials: BL
authors.lastname: Bassler
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology / Q000502:physiology*; D002628:Chemoreceptor Cells / Q000502:physiology*; D002633:Chemotaxis; D007659:Ketones / Q000737:chemistry / Q000378:metabolism*; D053038:Quorum Sensing; D014734:Vibrio cholerae / Q000378:metabolism
chemical_list: C525620:3-hydroxytridecan-4-one; D007659:Ketones
keywords: Bacterial Signal Transduction; Caenorhabditis elegans (C. elegans); Chemotaxis; Gene Regulation; Quorum Sensing; V. cholerae
references.citation: Nature. 2002 Jan 31;415(6871):545-9
references.pmid: 11823863
references.citation: Cell. 1997 Oct 17;91(2):161-9
references.pmid: 9346234
references.citation: Nat Neurosci. 2013 Oct;16(10):1461-7
references.pmid: 24013594
references.citation: Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1639-44
references.pmid: 9990077
references.citation: Dev Biol. 1984 Apr;102(2):368-78
references.pmid: 6706004
references.citation: Proc Natl Acad Sci U S A. 2010 Mar 23;107(12):5575-80
references.pmid: 20212168
references.citation: J Bacteriol. 2008 Apr;190(7):2527-36
references.pmid: 18223081
references.citation: Appl Environ Microbiol. 2006 Jul;72(7):5135-7
references.pmid: 16820523
references.citation: Nature. 2001 Apr 5;410(6829):698-701
references.pmid: 11287957
references.citation: Bioorg Med Chem. 2011 Nov 15;19(22):6906-18
references.pmid: 22001326
references.citation: J Bacteriol. 2004 Oct;186(20):6902-14
references.pmid: 15466044
references.citation: Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2295-300
references.pmid: 17267603
references.citation: Chem Biodivers. 2010 Aug;7(8):2016-22
references.pmid: 20730964
references.citation: J Exp Zool. 1974 Apr;188(1):41-7
references.pmid: 4822548
references.citation: Nature. 2005 Nov 10;438(7065):179-84
references.pmid: 16281027
references.citation: Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7046-50
references.pmid: 9618536
references.citation: Cell. 2007 May 18;129(4):787-99
references.pmid: 17512411
references.citation: WormBook. 2006 Oct 25;:1-29
references.pmid: 18050433
references.citation: Nature. 2005 Feb 3;433(7025):541-5
references.pmid: 15690045
references.citation: Cell. 2001 Apr 20;105(2):221-32
references.pmid: 11336672
references.citation: EMBO J. 2003 Feb 17;22(4):870-81
references.pmid: 12574123
references.citation: J Mol Biol. 1969 May 14;41(3):459-72
references.pmid: 4896022
references.citation: Mol Microbiol. 2001 Jul;41(2):463-76
references.pmid: 11489131
references.citation: Nature. 2008 Aug 28;454(7208):1115-8
references.pmid: 18650807
references.citation: Nature. 2007 Dec 6;450(7171):883-6
references.pmid: 18004304
references.citation: Biomed Eng Online. 2003 May 17;2:13
references.pmid: 12801419
references.citation: Cell. 2002 Aug 9;110(3):303-14
references.pmid: 12176318
references.citation: Cell. 1999 Nov 12;99(4):387-98
references.pmid: 10571181
references.citation: Science. 1990 Apr 6;248(4951):73-6
references.pmid: 2321027
references.citation: J Biol Chem. 2013 Jun 28;288(26):18778-83
references.pmid: 23689506
references.citation: J Comp Neurol. 1977 Apr 1;172(3):489-510
references.pmid: 838889
references.citation: Proc Natl Acad Sci U S A. 2009 Feb 10;106(6):1875-9
references.pmid: 19174521
references.citation: J Exp Zool. 1990 Mar;253(3):263-70
references.pmid: 2181052
references.citation: Dev Cell. 2003 Oct;5(4):621-33
references.pmid: 14536063
references.citation: Nat Chem Biol. 2007 Jul;3(7):420-2
references.pmid: 17558398
references.citation: Genetics. 1974 May;77(1):71-94
references.pmid: 4366476
references.citation: J Bacteriol. 2009 Jan;191(1):169-77
references.pmid: 18952786
references.citation: Proc Natl Acad Sci U S A. 2012 Dec 18;109(51):20949-54
references.pmid: 23213209
references.citation: Nat Chem Biol. 2009 Dec;5(12):891-5
references.pmid: 19838203
references.citation: Genetics. 1990 Apr;124(4):855-72
references.pmid: 2323555
references.citation: Mol Microbiol. 2011 Mar;79(6):1407-17
references.pmid: 21219472
references.citation: Mol Cell. 2009 Jul 31;35(2):143-53
references.pmid: 19647512
references.citation: Genes Dev. 2003 Sep 1;17(17):2123-37
references.pmid: 12952888
references.citation: Cell. 1993 Aug 13;74(3):515-27
references.pmid: 8348618
references.citation: Infect Immun. 1996 Jul;64(7):2853-6
references.pmid: 8698524
references.citation: Development. 2003 Apr;130(7):1215-24
references.pmid: 12588839
references.citation: Proc Natl Acad Sci U S A. 2010 Sep 21;107(38):16631-6
references.pmid: 20733068
references.citation: Proc Natl Acad Sci U S A. 1973 Mar;70(3):817-21
references.pmid: 4351805
references.citation: ACS Chem Biol. 2011 Apr 15;6(4):356-65
references.pmid: 21197957
references.citation: Science. 1982 May 28;216(4549):1012-4
references.pmid: 6805073