Pathogenic bacteria modulate pheromone response to promote mating
Pathogens generate ubiquitous selective pressures and host–pathogen interactions alter social behaviours in many animals 1 – 4 . However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behaviour. Here we show that in adult Caenorhabditis elegans herm...
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Published in | Nature (London) Vol. 613; no. 7943; pp. 324 - 331 |
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Main Authors | , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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London
Nature Publishing Group UK
12.01.2023
Nature Publishing Group |
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Abstract | Pathogens generate ubiquitous selective pressures and host–pathogen interactions alter social behaviours in many animals
1
–
4
. However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behaviour. Here we show that in adult
Caenorhabditis elegans
hermaphrodites, exposure to a bacterial pathogen (
Pseudomonas aeruginosa
) modulates sensory responses to pheromones by inducing the expression of the chemoreceptor STR-44 to promote mating. Under standard conditions,
C. elegans
hermaphrodites avoid a mixture of ascaroside pheromones to facilitate dispersal
5
–
13
. We find that exposure to the pathogenic
Pseudomonas
bacteria enables pheromone responses in AWA sensory neurons, which mediate attractive chemotaxis, to suppress the avoidance. Pathogen exposure induces
str-44
expression in AWA neurons, a process regulated by a transcription factor
zip-5
that also displays a pathogen-induced increase in expression in AWA. STR-44 acts as a pheromone receptor and its function in AWA neurons is required for pathogen-induced AWA pheromone response and suppression of pheromone avoidance. Furthermore, we show that
C. elegans
hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and that this increase requires
str-44
in AWA neurons. Thus, our results uncover a causal mechanism for pathogen-induced social behaviour plasticity, which can promote genetic diversity and facilitate adaptation of the host animals.
Infection of
Caenorhabditis elegans
by
Pseudomonas aeruginosa
causes an increased pheromone response via the pheromone receptor STR-44 and increases mating with males, a potential mechanism for promoting adaptation in the host. |
---|---|
AbstractList | Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and that this increase requires str-44 in AWA neurons. [...]our results uncover a causal mechanism for pathogen-induced social behaviour plasticity, which can promote genetic diversity and facilitate adaptation of the host animals. Ingestion of PA14 leads to intestinal infection and death of the worms within a few days23. [...]our results identified a type of social behavioural plasticity induced by exposure to pathogenic bacteria to suppress pheromone avoidance in C. elegans hermaphrodites. Together, these results suggest that these chemoreceptors do not regulate the pathogen-induced AWA response to the mixture of ascr#2, ascr#3 and ascr#5 in adult hermaphrodites. Because the previously identified receptors for ascarosides are chemoreceptors16,17,19-22,31, we reasoned that exposure to either PA14 or PA14-gacA(-) (Fig. 1f-h) would induce the expression of an unknown chemoreceptor that elicits the pheromone response of AWA neurons to suppress avoidance, but exposure to P.fluorescens would not (Extended Data Fig. 4b,c). [...]we performed translating ribosome Pathogens generate ubiquitous selective pressures and host-pathogen interactions alter social behaviours in many animals1-4. However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behaviour. Here we show that in adult Caenorhabditis elegans hermaphrodites, exposure to a bacterial pathogen (Pseudomonas aeruginosa) modulates sensory responses to pheromones by inducing the expression of the chemoreceptor STR-44 to promote mating. Under standard conditions, C. elegans hermaphrodites avoid a mixture of ascaroside pheromones to facilitate dispersal5-13. We find that exposure to the pathogenic Pseudomonas bacteria enables pheromone responses in AWA sensory neurons, which mediate attractive chemotaxis, to suppress the avoidance. Pathogen exposure induces str-44 expression in AWA neurons, a process regulated by a transcription factor zip-5 that also displays a pathogen-induced increase in expression in AWA. STR-44 acts as a pheromone receptor and its function in AWA neurons is required for pathogen-induced AWA pheromone response and suppression of pheromone avoidance. Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and that this increase requires str-44 in AWA neurons. Thus, our results uncover a causal mechanism for pathogen-induced social behaviour plasticity, which can promote genetic diversity and facilitate adaptation of the host animals. Pathogens generate ubiquitous selective pressures and host–pathogen interactions alter social behaviours in many animals 1 – 4 . However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behaviour. Here we show that in adult Caenorhabditis elegans hermaphrodites, exposure to a bacterial pathogen ( Pseudomonas aeruginosa ) modulates sensory responses to pheromones by inducing the expression of the chemoreceptor STR-44 to promote mating. Under standard conditions, C. elegans hermaphrodites avoid a mixture of ascaroside pheromones to facilitate dispersal 5 – 13 . We find that exposure to the pathogenic Pseudomonas bacteria enables pheromone responses in AWA sensory neurons, which mediate attractive chemotaxis, to suppress the avoidance. Pathogen exposure induces str-44 expression in AWA neurons, a process regulated by a transcription factor zip-5 that also displays a pathogen-induced increase in expression in AWA. STR-44 acts as a pheromone receptor and its function in AWA neurons is required for pathogen-induced AWA pheromone response and suppression of pheromone avoidance. Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and that this increase requires str-44 in AWA neurons. Thus, our results uncover a causal mechanism for pathogen-induced social behaviour plasticity, which can promote genetic diversity and facilitate adaptation of the host animals. Infection of Caenorhabditis elegans by Pseudomonas aeruginosa causes an increased pheromone response via the pheromone receptor STR-44 and increases mating with males, a potential mechanism for promoting adaptation in the host. Pathogens generate ubiquitous selective pressures and host-pathogen interactions alter social behaviors in many animals 1 – 4 . However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behavior. Here we show that in adult Caenorhabditis elegans hermaphrodites, exposure to a bacterial pathogen ( Pseudomonas aeruginosa ) modulates sensory responses to pheromones by inducing the expression of a chemoreceptor STR-44 to promote mating. Under standard conditions, C. elegans hermaphrodites avoid a mixture of ascaroside pheromones to facilitate dispersal 5 – 13 . We find that exposure to the pathogenic Pseudomonas bacteria enables pheromone responses in AWA sensory neurons, which mediate attractive chemotaxis, to suppress the avoidance. Pathogen exposure induces str-44 expression in AWA, a process regulated by a transcription factor zip-5 that also displays a pathogen-induced increase in AWA expression. STR-44 acts as a pheromone receptor and its function in AWA is required for pathogen-induced AWA pheromone response and suppression of pheromone avoidance. Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and this increase requires str-44 in AWA. Thus, our results discover a causal mechanism for pathogen-induced social behavior plasticity, which can promote genetic diversity and facilitate adaptation of the host animals. Pathogens generate ubiquitous selective pressures and host-pathogen interactions alter social behaviours in many animals . However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behaviour. Here we show that in adult Caenorhabditis elegans hermaphrodites, exposure to a bacterial pathogen (Pseudomonas aeruginosa) modulates sensory responses to pheromones by inducing the expression of the chemoreceptor STR-44 to promote mating. Under standard conditions, C. elegans hermaphrodites avoid a mixture of ascaroside pheromones to facilitate dispersal . We find that exposure to the pathogenic Pseudomonas bacteria enables pheromone responses in AWA sensory neurons, which mediate attractive chemotaxis, to suppress the avoidance. Pathogen exposure induces str-44 expression in AWA neurons, a process regulated by a transcription factor zip-5 that also displays a pathogen-induced increase in expression in AWA. STR-44 acts as a pheromone receptor and its function in AWA neurons is required for pathogen-induced AWA pheromone response and suppression of pheromone avoidance. Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and that this increase requires str-44 in AWA neurons. Thus, our results uncover a causal mechanism for pathogen-induced social behaviour plasticity, which can promote genetic diversity and facilitate adaptation of the host animals. |
Author | Wu, Min Duan, Fengyun Yang, Wenxing Liu, He Chen, Maoting Gracida, Xicotencatl Saltzman, Arneet L. Zhang, Yun Li, Chengyin Ge, Minghai Liang, Jingting Wu, Taihong Dar, Abdul Rouf Butcher, Rebecca A. |
AuthorAffiliation | 4 Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada 1 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA 2 Center for Brain Science, Harvard University, Cambridge, MA, USA 3 Department of Chemistry, University of Florida, Gainesville, FL, USA |
AuthorAffiliation_xml | – name: 3 Department of Chemistry, University of Florida, Gainesville, FL, USA – name: 1 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA – name: 2 Center for Brain Science, Harvard University, Cambridge, MA, USA – name: 4 Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada |
Author_xml | – sequence: 1 givenname: Taihong orcidid: 0000-0002-9760-6978 surname: Wu fullname: Wu, Taihong organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 2 givenname: Minghai surname: Ge fullname: Ge, Minghai organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 3 givenname: Min orcidid: 0000-0002-4059-1234 surname: Wu fullname: Wu, Min organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 4 givenname: Fengyun surname: Duan fullname: Duan, Fengyun organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 5 givenname: Jingting surname: Liang fullname: Liang, Jingting organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 6 givenname: Maoting surname: Chen fullname: Chen, Maoting organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 7 givenname: Xicotencatl surname: Gracida fullname: Gracida, Xicotencatl organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 8 givenname: He surname: Liu fullname: Liu, He organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 9 givenname: Wenxing surname: Yang fullname: Yang, Wenxing organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University – sequence: 10 givenname: Abdul Rouf surname: Dar fullname: Dar, Abdul Rouf organization: Department of Chemistry, University of Florida – sequence: 11 givenname: Chengyin orcidid: 0000-0001-8543-3419 surname: Li fullname: Li, Chengyin organization: Department of Cell and Systems Biology, University of Toronto – sequence: 12 givenname: Rebecca A. orcidid: 0000-0002-0925-4459 surname: Butcher fullname: Butcher, Rebecca A. organization: Department of Chemistry, University of Florida – sequence: 13 givenname: Arneet L. surname: Saltzman fullname: Saltzman, Arneet L. organization: Department of Cell and Systems Biology, University of Toronto – sequence: 14 givenname: Yun orcidid: 0000-0002-7631-858X surname: Zhang fullname: Zhang, Yun email: yzhang@oeb.harvard.edu organization: Department of Organismic and Evolutionary Biology, Harvard University, Center for Brain Science, Harvard University |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36599989$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions. T.W., M.G. and Y.Z. conceived the study and designed the experiments. T.W., M.G., F.D., J.L. and W.Y. performed behavioral assays, calcium imaging and gene expression analysis and analyzed data. T.W., F.D., X.G., and H.L. generated TRAP-RNAseq samples; T.W., M.W., and M.C. analyzed the TRAP-RNAseq data. A.R.D. and R.A.B. generated pheromones for the study. T.W., M.G., C.L., A.L.S. and Y.Z. designed ChIP-qPCR experiments. T.W. and M.G. collected samples for ChIP-qPCR assays, and C.L. and A.L.S. performed ChIP-qPCR and analyzed data. T.W., M.G., M.W., C.L., A.L.S. and Y.Z. wrote the paper. All authors discussed the results and commented on the manuscript. These authors contribute equally. |
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PublicationDate | 2023-01-12 |
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Snippet | Pathogens generate ubiquitous selective pressures and host–pathogen interactions alter social behaviours in many animals
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. However, very little is known... Pathogens generate ubiquitous selective pressures and host-pathogen interactions alter social behaviours in many animals . However, very little is known about... Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen... Pathogens generate ubiquitous selective pressures and host-pathogen interactions alter social behaviours in many animals1-4. However, very little is known... Pathogens generate ubiquitous selective pressures and host-pathogen interactions alter social behaviors in many animals 1 – 4 . However, very little is known... |
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SubjectTerms | 14/19 38 38/35 38/91 631/378/3917 631/378/3919 64/11 Animals Avoidance Bacteria Caenorhabditis elegans - metabolism Caenorhabditis elegans - microbiology Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - metabolism Chemoreceptors E coli Exposure Female Fertilization Genetic diversity Glycolipids - metabolism Hermaphrodites Hermaphroditic Organisms - physiology Histamine Humanities and Social Sciences Ingestion Male Mating multidisciplinary Neurons Pathogens Pheromones Pheromones - metabolism Plasticity Pseudomonas aeruginosa - pathogenicity Pseudomonas aeruginosa - physiology Receptors, Pheromone - metabolism Reproduction - physiology Science Science (multidisciplinary) Self-fertilization Sensory Receptor Cells - metabolism Sexual Behavior, Animal Social behavior Worms |
Title | Pathogenic bacteria modulate pheromone response to promote mating |
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