The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut
Summary: Chronic stress disrupts microbiota-gut-brain axis function and is associated with altered tryptophan metabolism, impaired gut barrier function, and disrupted diurnal rhythms. However, little is known about the effects of acute stress on the gut and how it is influenced by diurnal physiology...
| Main Authors: | , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2024-04-01
|
| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724004078 |
| _version_ | 1797210015090606080 |
|---|---|
| author | Cassandra E. Gheorghe Sarah-Jane Leigh Gabriel S.S. Tofani Thomaz F.S. Bastiaanssen Joshua M. Lyte Elisa Gardellin Ashokkumar Govindan Conall Strain Sonia Martinez-Herrero Michael S. Goodson Nancy Kelley-Loughnane John F. Cryan Gerard Clarke |
| author_facet | Cassandra E. Gheorghe Sarah-Jane Leigh Gabriel S.S. Tofani Thomaz F.S. Bastiaanssen Joshua M. Lyte Elisa Gardellin Ashokkumar Govindan Conall Strain Sonia Martinez-Herrero Michael S. Goodson Nancy Kelley-Loughnane John F. Cryan Gerard Clarke |
| author_sort | Cassandra E. Gheorghe |
| collection | DOAJ |
| description | Summary: Chronic stress disrupts microbiota-gut-brain axis function and is associated with altered tryptophan metabolism, impaired gut barrier function, and disrupted diurnal rhythms. However, little is known about the effects of acute stress on the gut and how it is influenced by diurnal physiology. Here, we used germ-free and antibiotic-depleted mice to understand how microbiota-dependent oscillations in tryptophan metabolism would alter gut barrier function at baseline and in response to an acute stressor. Cecal metabolomics identified tryptophan metabolism as most responsive to a 15-min acute stressor, while shotgun metagenomics revealed that most bacterial species exhibiting rhythmicity metabolize tryptophan. Our findings highlight that the gastrointestinal response to acute stress is dependent on the time of day and the microbiome, with a signature of stress-induced functional alterations in the ileum and altered tryptophan metabolism in the colon. |
| first_indexed | 2024-04-24T10:03:52Z |
| format | Article |
| id | doaj.art-2451a00d25244e4ea04d5c872d5038b9 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-24T10:03:52Z |
| publishDate | 2024-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-2451a00d25244e4ea04d5c872d5038b92024-04-13T04:21:13ZengElsevierCell Reports2211-12472024-04-01434114079The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gutCassandra E. Gheorghe0Sarah-Jane Leigh1Gabriel S.S. Tofani2Thomaz F.S. Bastiaanssen3Joshua M. Lyte4Elisa Gardellin5Ashokkumar Govindan6Conall Strain7Sonia Martinez-Herrero8Michael S. Goodson9Nancy Kelley-Loughnane10John F. Cryan11Gerard Clarke12APC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Teagasc Moorepark Food Research Centre, Fermoy Co, P61 C996 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Teagasc Moorepark Food Research Centre, Fermoy Co, P61 C996 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, Ireland711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson Air Force Base, Dayton, OH 45324, USA711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson Air Force Base, Dayton, OH 45324, USAAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, T12 CY82 Cork, IrelandAPC Microbiome Ireland, University College Cork, T12 CY82 Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, T12 CY82 Cork, Ireland; Corresponding authorSummary: Chronic stress disrupts microbiota-gut-brain axis function and is associated with altered tryptophan metabolism, impaired gut barrier function, and disrupted diurnal rhythms. However, little is known about the effects of acute stress on the gut and how it is influenced by diurnal physiology. Here, we used germ-free and antibiotic-depleted mice to understand how microbiota-dependent oscillations in tryptophan metabolism would alter gut barrier function at baseline and in response to an acute stressor. Cecal metabolomics identified tryptophan metabolism as most responsive to a 15-min acute stressor, while shotgun metagenomics revealed that most bacterial species exhibiting rhythmicity metabolize tryptophan. Our findings highlight that the gastrointestinal response to acute stress is dependent on the time of day and the microbiome, with a signature of stress-induced functional alterations in the ileum and altered tryptophan metabolism in the colon.http://www.sciencedirect.com/science/article/pii/S2211124724004078CP: MicrobiologyCP: Metabolism |
| spellingShingle | Cassandra E. Gheorghe Sarah-Jane Leigh Gabriel S.S. Tofani Thomaz F.S. Bastiaanssen Joshua M. Lyte Elisa Gardellin Ashokkumar Govindan Conall Strain Sonia Martinez-Herrero Michael S. Goodson Nancy Kelley-Loughnane John F. Cryan Gerard Clarke The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut Cell Reports CP: Microbiology CP: Metabolism |
| title | The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut |
| title_full | The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut |
| title_fullStr | The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut |
| title_full_unstemmed | The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut |
| title_short | The microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut |
| title_sort | microbiota drives diurnal rhythms in tryptophan metabolism in the stressed gut |
| topic | CP: Microbiology CP: Metabolism |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724004078 |
| work_keys_str_mv | AT cassandraegheorghe themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT sarahjaneleigh themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT gabrielsstofani themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT thomazfsbastiaanssen themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT joshuamlyte themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT elisagardellin themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT ashokkumargovindan themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT conallstrain themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT soniamartinezherrero themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT michaelsgoodson themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT nancykelleyloughnane themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT johnfcryan themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT gerardclarke themicrobiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT cassandraegheorghe microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT sarahjaneleigh microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT gabrielsstofani microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT thomazfsbastiaanssen microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT joshuamlyte microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT elisagardellin microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT ashokkumargovindan microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT conallstrain microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT soniamartinezherrero microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT michaelsgoodson microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT nancykelleyloughnane microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT johnfcryan microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut AT gerardclarke microbiotadrivesdiurnalrhythmsintryptophanmetabolisminthestressedgut |