L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human
ABSTRACTFermented foods and beverages are a significant source of dietary bacteria that enter the gastrointestinal (GI) tract. However, little is known about how these microbes survive and adapt to the small intestinal environment. Colony-forming units (CFU) enumeration and viability qPCR of Lactica...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2023-12-01
|
| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2244720 |
| _version_ | 1827303772568682496 |
|---|---|
| author | Edoardo Zaccaria Tim Klaassen Annick M.E. Alleleyn Jos Boekhorst Christian Chervaux Tamara Smokvina Freddy J. Troost Michiel Kleerebezem |
| author_facet | Edoardo Zaccaria Tim Klaassen Annick M.E. Alleleyn Jos Boekhorst Christian Chervaux Tamara Smokvina Freddy J. Troost Michiel Kleerebezem |
| author_sort | Edoardo Zaccaria |
| collection | DOAJ |
| description | ABSTRACTFermented foods and beverages are a significant source of dietary bacteria that enter the gastrointestinal (GI) tract. However, little is known about how these microbes survive and adapt to the small intestinal environment. Colony-forming units (CFU) enumeration and viability qPCR of Lacticaseibacillus rhamnosus CNCM I-3690 in the ileal effluent of 10 ileostomy subjects during 12-h post consumption of a dairy product fermented with this strain demonstrated the high level of survival of this strain during human small intestine passage. Metatranscriptome analyses revealed the in situ transcriptome of L. rhamnosus in the small intestine, which was contrasted with transcriptome data obtained from in vitro cultivation. These comparative analyses revealed substantial metabolic adaptations of L. rhamnosus during small intestine transit, including adjustments of carbohydrate metabolism, surface-protein expression, and translation machinery. The prominent presence of L. rhamnosus in the effluent samples did not elicit an appreciable effect on the composition of the endogenous small intestine microbiome, but significantly altered the ecosystem’s overall activity profile, particularly of pathways associated with carbohydrate metabolism. Strikingly, two of the previously recognized gut-brain metabolic modules expressed in situ by L. rhamnosus (inositol degradation and glutamate synthesis II) are among the most dominantly enriched activities in the ecosystem’s activity profile. This study establishes the survival capacity of L. rhamnosus in the human small intestine and highlights its functional adjustment in situ, which we postulate to play a role in the probiotic effects associated with this strain. |
| first_indexed | 2024-03-11T14:19:54Z |
| format | Article |
| id | doaj.art-037894a2ef0c4dcebe9b6ea0161797ff |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-24T17:06:49Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-037894a2ef0c4dcebe9b6ea0161797ff2024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2244720L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in humanEdoardo Zaccaria0Tim Klaassen1Annick M.E. Alleleyn2Jos Boekhorst3Christian Chervaux4Tamara Smokvina5Freddy J. Troost6Michiel Kleerebezem7Host Microbe Interactomics Group, Wageningen University & Research, Wageningen, The NetherlandsDivision of Gastroenterology-Hepatology, Department of Internal Medicine, School of Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University Medical Center+, Maastricht, The NetherlandsFood Innovation and Health, Department of Human Biology, School of Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University, Venlo, The NetherlandsHost Microbe Interactomics Group, Wageningen University & Research, Wageningen, The NetherlandsDanone Nutricia Research, Centre Daniel Carasso, Palaiseau, FranceDanone Nutricia Research, Centre Daniel Carasso, Palaiseau, FranceDivision of Gastroenterology-Hepatology, Department of Internal Medicine, School of Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University Medical Center+, Maastricht, The NetherlandsHost Microbe Interactomics Group, Wageningen University & Research, Wageningen, The NetherlandsABSTRACTFermented foods and beverages are a significant source of dietary bacteria that enter the gastrointestinal (GI) tract. However, little is known about how these microbes survive and adapt to the small intestinal environment. Colony-forming units (CFU) enumeration and viability qPCR of Lacticaseibacillus rhamnosus CNCM I-3690 in the ileal effluent of 10 ileostomy subjects during 12-h post consumption of a dairy product fermented with this strain demonstrated the high level of survival of this strain during human small intestine passage. Metatranscriptome analyses revealed the in situ transcriptome of L. rhamnosus in the small intestine, which was contrasted with transcriptome data obtained from in vitro cultivation. These comparative analyses revealed substantial metabolic adaptations of L. rhamnosus during small intestine transit, including adjustments of carbohydrate metabolism, surface-protein expression, and translation machinery. The prominent presence of L. rhamnosus in the effluent samples did not elicit an appreciable effect on the composition of the endogenous small intestine microbiome, but significantly altered the ecosystem’s overall activity profile, particularly of pathways associated with carbohydrate metabolism. Strikingly, two of the previously recognized gut-brain metabolic modules expressed in situ by L. rhamnosus (inositol degradation and glutamate synthesis II) are among the most dominantly enriched activities in the ecosystem’s activity profile. This study establishes the survival capacity of L. rhamnosus in the human small intestine and highlights its functional adjustment in situ, which we postulate to play a role in the probiotic effects associated with this strain.https://www.tandfonline.com/doi/10.1080/19490976.2023.2244720L. rhamnosussmall intestinehumanmetatranscriptomein situ gene expressionprobiotic fate |
| spellingShingle | Edoardo Zaccaria Tim Klaassen Annick M.E. Alleleyn Jos Boekhorst Christian Chervaux Tamara Smokvina Freddy J. Troost Michiel Kleerebezem L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human Gut Microbes L. rhamnosus small intestine human metatranscriptome in situ gene expression probiotic fate |
| title | L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human |
| title_full | L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human |
| title_fullStr | L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human |
| title_full_unstemmed | L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human |
| title_short | L. rhamnosus CNCM I-3690 survival, adaptation, and small bowel microbiome impact in human |
| title_sort | l rhamnosus cncm i 3690 survival adaptation and small bowel microbiome impact in human |
| topic | L. rhamnosus small intestine human metatranscriptome in situ gene expression probiotic fate |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2244720 |
| work_keys_str_mv | AT edoardozaccaria lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT timklaassen lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT annickmealleleyn lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT josboekhorst lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT christianchervaux lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT tamarasmokvina lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT freddyjtroost lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman AT michielkleerebezem lrhamnosuscncmi3690survivaladaptationandsmallbowelmicrobiomeimpactinhuman |