Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber
Abstract While deprivation of dietary fiber has been associated with adverse health outcomes, investigations concerning the effect of dietary fiber on the gut microbiome have been largely limited to compositional sequence-based analyses or utilize a defined microbiota not native to the host. To exte...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2022-07-01
|
| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-022-00313-z |
| _version_ | 1817968912361324544 |
|---|---|
| author | Bryan J. Killinger Christopher Whidbey Natalie C. Sadler Adrian J. DeLeon Nathalie Munoz Young-Mo Kim Aaron T. Wright |
| author_facet | Bryan J. Killinger Christopher Whidbey Natalie C. Sadler Adrian J. DeLeon Nathalie Munoz Young-Mo Kim Aaron T. Wright |
| author_sort | Bryan J. Killinger |
| collection | DOAJ |
| description | Abstract While deprivation of dietary fiber has been associated with adverse health outcomes, investigations concerning the effect of dietary fiber on the gut microbiome have been largely limited to compositional sequence-based analyses or utilize a defined microbiota not native to the host. To extend understanding of the microbiome’s functional response to dietary fiber deprivation beyond correlative evidence from sequence-based analyses, approaches capable of measuring functional enzymatic activity are needed. In this study, we use an activity-based protein profiling (ABPP) approach to identify sugar metabolizing and transport proteins in native mouse gut microbiomes that respond with differential activity to the deprivation or supplementation of the soluble dietary fibers inulin and pectin. We found that the microbiome of mice subjected to a high fiber diet high in soluble fiber had increased functional activity of multiple proteins, including glycoside hydrolases, polysaccharide lyases, and sugar transport proteins from diverse taxa. The results point to an increase in activity of the Bifidobacterium shunt metabolic pathway in the microbiome of mice fed high fiber diets. In those subjected to a low fiber diet, we identified a shift from the degradation of dietary fibers to that of gut mucins, in particular by the recently isolated taxon “Musculibacterium intestinale”, which experienced dramatic growth in response to fiber deprivation. When combined with metabolomics and shotgun metagenomics analyses, our findings provide a functional investigation of dietary fiber metabolism in the gut microbiome and demonstrates the power of a combined ABPP-multiomics approach for characterizing the response of the gut microbiome to perturbations. |
| first_indexed | 2024-04-13T20:13:56Z |
| format | Article |
| id | doaj.art-bc65aa0687a3432ca6dad29598eb4b9e |
| institution | Directory Open Access Journal |
| issn | 2055-5008 |
| language | English |
| last_indexed | 2024-04-13T20:13:56Z |
| publishDate | 2022-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj.art-bc65aa0687a3432ca6dad29598eb4b9e2022-12-22T02:31:45ZengNature Portfolionpj Biofilms and Microbiomes2055-50082022-07-018111010.1038/s41522-022-00313-zActivity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiberBryan J. Killinger0Christopher Whidbey1Natalie C. Sadler2Adrian J. DeLeon3Nathalie Munoz4Young-Mo Kim5Aaron T. Wright6Biological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryAbstract While deprivation of dietary fiber has been associated with adverse health outcomes, investigations concerning the effect of dietary fiber on the gut microbiome have been largely limited to compositional sequence-based analyses or utilize a defined microbiota not native to the host. To extend understanding of the microbiome’s functional response to dietary fiber deprivation beyond correlative evidence from sequence-based analyses, approaches capable of measuring functional enzymatic activity are needed. In this study, we use an activity-based protein profiling (ABPP) approach to identify sugar metabolizing and transport proteins in native mouse gut microbiomes that respond with differential activity to the deprivation or supplementation of the soluble dietary fibers inulin and pectin. We found that the microbiome of mice subjected to a high fiber diet high in soluble fiber had increased functional activity of multiple proteins, including glycoside hydrolases, polysaccharide lyases, and sugar transport proteins from diverse taxa. The results point to an increase in activity of the Bifidobacterium shunt metabolic pathway in the microbiome of mice fed high fiber diets. In those subjected to a low fiber diet, we identified a shift from the degradation of dietary fibers to that of gut mucins, in particular by the recently isolated taxon “Musculibacterium intestinale”, which experienced dramatic growth in response to fiber deprivation. When combined with metabolomics and shotgun metagenomics analyses, our findings provide a functional investigation of dietary fiber metabolism in the gut microbiome and demonstrates the power of a combined ABPP-multiomics approach for characterizing the response of the gut microbiome to perturbations.https://doi.org/10.1038/s41522-022-00313-z |
| spellingShingle | Bryan J. Killinger Christopher Whidbey Natalie C. Sadler Adrian J. DeLeon Nathalie Munoz Young-Mo Kim Aaron T. Wright Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber npj Biofilms and Microbiomes |
| title | Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber |
| title_full | Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber |
| title_fullStr | Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber |
| title_full_unstemmed | Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber |
| title_short | Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber |
| title_sort | activity based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber |
| url | https://doi.org/10.1038/s41522-022-00313-z |
| work_keys_str_mv | AT bryanjkillinger activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber AT christopherwhidbey activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber AT nataliecsadler activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber AT adrianjdeleon activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber AT nathaliemunoz activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber AT youngmokim activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber AT aarontwright activitybasedproteinprofilingidentifiesalternatingactivationofenzymesinvolvedinthebifidobacteriumshuntpathwayormucindegradationinthegutmicrobiomeresponsetosolubledietaryfiber |