Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample
ABSTRACT Dietary fibers influence the composition of the human gut microbiota and directly contribute to its downstream effects on host health. As more research supports the use of glycans as prebiotics for therapeutic applications, the need to identify the gut bacteria that metabolize glycans of in...
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American Society for Microbiology
2025-01-01
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| Series: | mSphere |
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| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00668-24 |
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| author | Catherine Prattico Emmanuel Gonzalez Lharbi Dridi Shiva Jazestani Kristin E. Low D. Wade Abbott Corinne F. Maurice Bastien Castagner |
| author_facet | Catherine Prattico Emmanuel Gonzalez Lharbi Dridi Shiva Jazestani Kristin E. Low D. Wade Abbott Corinne F. Maurice Bastien Castagner |
| author_sort | Catherine Prattico |
| collection | DOAJ |
| description | ABSTRACT Dietary fibers influence the composition of the human gut microbiota and directly contribute to its downstream effects on host health. As more research supports the use of glycans as prebiotics for therapeutic applications, the need to identify the gut bacteria that metabolize glycans of interest increases. Fructo-oligosaccharide (FOS) is a common diet-derived glycan that is fermented by the gut microbiota and has been used as a prebiotic. Despite being well studied, we do not yet have a complete picture of all FOS-consuming gut bacterial taxa. To identify new bacterial consumers, we used a short exposure of microbial communities in a stool sample to FOS or galactomannan as the sole carbon source to induce glycan metabolism genes. We then performed metatranscriptomics, paired with whole metagenomic sequencing, and 16S amplicon sequencing. The short incubation was sufficient to cause induction of genes involved in carbohydrate metabolism, like carbohydrate-active enzymes (CAZymes), including glycoside hydrolase family 32 genes, which hydrolyze fructan polysaccharides like FOS and inulin. Interestingly, FOS metabolism transcripts were notably overexpressed in Blautia species not previously reported to be fructan consumers. We therefore validated the ability of different Blautia species to ferment fructans by monitoring their growth and fermentation in defined media. This pulse metatranscriptomics approach is a useful method to find novel consumers of prebiotics and increase our understanding of prebiotic metabolism by CAZymes in the gut microbiota.IMPORTANCEComplex carbohydrates are key contributors to the composition of the human gut microbiota and play an essential role in the microbiota’s effects on host health. Understanding which bacteria consume complex carbohydrates, or glycans, provides a mechanistic link between dietary prebiotics and their beneficial health effects, an essential step for their therapeutic application. Here, we used a pulse metatranscriptomics pipeline to identify bacterial consumers based on glycan metabolism induction in a human stool sample. We identified novel consumers of fructo-oligosaccharide among Blautia species, expanding our understanding of this well-known glycan. Our approach can be applied to identify consumers of understudied glycans and expand our prebiotic repertoire. It can also be used to study prebiotic glycans directly in stool samples in distinct patient populations to help delineate the prebiotic mechanism. |
| format | Article |
| id | doaj-art-4fb97ba82971402792f1ab440aa53f31 |
| institution | Kabale University |
| issn | 2379-5042 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj-art-4fb97ba82971402792f1ab440aa53f312025-01-28T14:00:56ZengAmerican Society for MicrobiologymSphere2379-50422025-01-0110110.1128/msphere.00668-24Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sampleCatherine Prattico0Emmanuel Gonzalez1Lharbi Dridi2Shiva Jazestani3Kristin E. Low4D. Wade Abbott5Corinne F. Maurice6Bastien Castagner7Department of Microbiology & Immunology, Faculty of Medicine and Health Sciences, McGill University, Montréal, Québec, CanadaCanadian Centre for Computational Genomics, McGill Genome Centre, McGill University, Montréal, Québec, CanadaDepartment of Pharmacology & Therapeutics, Faculty of Medicine and Health Sciences, McGill University, Montréal, Québec, CanadaDepartment of Pharmacology & Therapeutics, Faculty of Medicine and Health Sciences, McGill University, Montréal, Québec, CanadaAgriculture and Agri-Food Canada, Lethbridge Research and Development Centre, Lethbridge, Alberta, CanadaAgriculture and Agri-Food Canada, Lethbridge Research and Development Centre, Lethbridge, Alberta, CanadaDepartment of Microbiology & Immunology, Faculty of Medicine and Health Sciences, McGill University, Montréal, Québec, CanadaDepartment of Pharmacology & Therapeutics, Faculty of Medicine and Health Sciences, McGill University, Montréal, Québec, CanadaABSTRACT Dietary fibers influence the composition of the human gut microbiota and directly contribute to its downstream effects on host health. As more research supports the use of glycans as prebiotics for therapeutic applications, the need to identify the gut bacteria that metabolize glycans of interest increases. Fructo-oligosaccharide (FOS) is a common diet-derived glycan that is fermented by the gut microbiota and has been used as a prebiotic. Despite being well studied, we do not yet have a complete picture of all FOS-consuming gut bacterial taxa. To identify new bacterial consumers, we used a short exposure of microbial communities in a stool sample to FOS or galactomannan as the sole carbon source to induce glycan metabolism genes. We then performed metatranscriptomics, paired with whole metagenomic sequencing, and 16S amplicon sequencing. The short incubation was sufficient to cause induction of genes involved in carbohydrate metabolism, like carbohydrate-active enzymes (CAZymes), including glycoside hydrolase family 32 genes, which hydrolyze fructan polysaccharides like FOS and inulin. Interestingly, FOS metabolism transcripts were notably overexpressed in Blautia species not previously reported to be fructan consumers. We therefore validated the ability of different Blautia species to ferment fructans by monitoring their growth and fermentation in defined media. This pulse metatranscriptomics approach is a useful method to find novel consumers of prebiotics and increase our understanding of prebiotic metabolism by CAZymes in the gut microbiota.IMPORTANCEComplex carbohydrates are key contributors to the composition of the human gut microbiota and play an essential role in the microbiota’s effects on host health. Understanding which bacteria consume complex carbohydrates, or glycans, provides a mechanistic link between dietary prebiotics and their beneficial health effects, an essential step for their therapeutic application. Here, we used a pulse metatranscriptomics pipeline to identify bacterial consumers based on glycan metabolism induction in a human stool sample. We identified novel consumers of fructo-oligosaccharide among Blautia species, expanding our understanding of this well-known glycan. Our approach can be applied to identify consumers of understudied glycans and expand our prebiotic repertoire. It can also be used to study prebiotic glycans directly in stool samples in distinct patient populations to help delineate the prebiotic mechanism.https://journals.asm.org/doi/10.1128/msphere.00668-24gut microbiomeprebioticsmetatranscriptomicsFOSgalactomannanCAZymes |
| spellingShingle | Catherine Prattico Emmanuel Gonzalez Lharbi Dridi Shiva Jazestani Kristin E. Low D. Wade Abbott Corinne F. Maurice Bastien Castagner Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample mSphere gut microbiome prebiotics metatranscriptomics FOS galactomannan CAZymes |
| title | Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample |
| title_full | Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample |
| title_fullStr | Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample |
| title_full_unstemmed | Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample |
| title_short | Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample |
| title_sort | identification of novel fructo oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample |
| topic | gut microbiome prebiotics metatranscriptomics FOS galactomannan CAZymes |
| url | https://journals.asm.org/doi/10.1128/msphere.00668-24 |
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