Modulation of sensory perception by hydrogen peroxide enables Caenorhabditis elegans to find a niche that provides both food and protection from hydrogen peroxide
Hydrogen peroxide (H2O2) is the most common chemical threat that organisms face. Here, we show that H2O2 alters the bacterial food preference of Caenorhabditis elegans, enabling the nematodes to find a safe environment with food. H2O2 induces the nematodes to leave food patches of laboratory and mic...
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| Veröffentlicht in: | PLoS pathogens 2021-12, Vol.17 (12), p.e1010112 |
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| creator | 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 Assié, Adrien Samuel, Buck S O'Donnell, Michael P Venkatachalam, Vivek Apfeld, Javier |
| description | Hydrogen peroxide (H2O2) is the most common chemical threat that organisms face. Here, we show that H2O2 alters the bacterial food preference of Caenorhabditis elegans, enabling the nematodes to find a safe environment with food. H2O2 induces the nematodes to leave food patches of laboratory and microbiome bacteria when those bacterial communities have insufficient H2O2-degrading capacity. The nematode's behavior is directed by H2O2-sensing neurons that promote escape from H2O2 and by bacteria-sensing neurons that promote attraction to bacteria. However, the input for H2O2-sensing neurons is removed by bacterial H2O2-degrading enzymes and the bacteria-sensing neurons' perception of bacteria is prevented by H2O2. 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. |
| doi_str_mv | 10.1371/journal.ppat.1010112 |
| format | Article |
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Here, we show that H2O2 alters the bacterial food preference of Caenorhabditis elegans, enabling the nematodes to find a safe environment with food. H2O2 induces the nematodes to leave food patches of laboratory and microbiome bacteria when those bacterial communities have insufficient H2O2-degrading capacity. The nematode's behavior is directed by H2O2-sensing neurons that promote escape from H2O2 and by bacteria-sensing neurons that promote attraction to bacteria. However, the input for H2O2-sensing neurons is removed by bacterial H2O2-degrading enzymes and the bacteria-sensing neurons' perception of bacteria is prevented by H2O2. 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Buck S</au><au>O'Donnell, Michael P</au><au>Venkatachalam, Vivek</au><au>Apfeld, Javier</au><au>Weaver, Benjamin</au><aucorp>USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modulation of sensory perception by hydrogen peroxide enables Caenorhabditis elegans to find a niche that provides both food and protection from hydrogen peroxide</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2021-12-23</date><risdate>2021</risdate><volume>17</volume><issue>12</issue><spage>e1010112</spage><pages>e1010112-</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Hydrogen peroxide (H2O2) is the most common chemical threat that organisms face. Here, we show that H2O2 alters the bacterial food preference of Caenorhabditis elegans, enabling the nematodes to find a safe environment with food. H2O2 induces the nematodes to leave food patches of laboratory and microbiome bacteria when those bacterial communities have insufficient H2O2-degrading capacity. The nematode's behavior is directed by H2O2-sensing neurons that promote escape from H2O2 and by bacteria-sensing neurons that promote attraction to bacteria. However, the input for H2O2-sensing neurons is removed by bacterial H2O2-degrading enzymes and the bacteria-sensing neurons' perception of bacteria is prevented by H2O2. 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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34941962</pmid><doi>10.1371/journal.ppat.1010112</doi><tpages>e1010112</tpages><orcidid>https://orcid.org/0000-0001-8313-8969</orcidid><orcidid>https://orcid.org/0000-0003-0265-1483</orcidid><orcidid>https://orcid.org/0000-0002-4541-5889</orcidid><orcidid>https://orcid.org/0000-0002-4381-0367</orcidid><orcidid>https://orcid.org/0000-0001-8551-5035</orcidid><orcidid>https://orcid.org/0000-0003-3335-1248</orcidid><orcidid>https://orcid.org/0000-0003-3568-0766</orcidid><orcidid>https://orcid.org/0000-0002-4347-3997</orcidid><orcidid>https://orcid.org/0000-0002-5461-4986</orcidid><orcidid>https://orcid.org/0000-0001-9897-5671</orcidid><orcidid>https://orcid.org/0000000254614986</orcidid><orcidid>https://orcid.org/0000000183138969</orcidid><orcidid>https://orcid.org/0000000302651483</orcidid><orcidid>https://orcid.org/0000000243473997</orcidid><orcidid>https://orcid.org/0000000333351248</orcidid><orcidid>https://orcid.org/0000000335680766</orcidid><orcidid>https://orcid.org/0000000198975671</orcidid><orcidid>https://orcid.org/0000000185515035</orcidid><orcidid>https://orcid.org/0000000245415889</orcidid><orcidid>https://orcid.org/0000000243810367</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7374 |
| ispartof | PLoS pathogens, 2021-12, Vol.17 (12), p.e1010112 |
| issn | 1553-7374 1553-7366 1553-7374 |
| language | eng |
| recordid | cdi_plos_journals_2620156050 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; PubMed Central Open Access; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | animal behavior Animal feeding behavior Animals Attenuation Bacteria Bacteria - metabolism BASIC BIOLOGICAL SCIENCES Behavior Behavior, Animal - physiology Biological research Biology and Life Sciences Biology, Experimental Caenorhabditis elegans Caenorhabditis elegans - physiology E coli Enzymes Escherichia coli Food Food preferences Host-bacteria relationships Hydrogen Hydrogen Peroxide Laboratories Locomotion - physiology Microbiomes Nematodes Neurons Perception Perception - physiology Physical Sciences Physiological aspects Research and Analysis Methods Sensory discrimination sensory neurons Sensory perception Sensory Receptor Cells - physiology Social Sciences Streptococcus infections Worms |
| title | Modulation of sensory perception by hydrogen peroxide enables Caenorhabditis elegans to find a niche that provides both food and protection from hydrogen peroxide |
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