Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits
Abstract Background Mammalian milk oligosaccharides serve as the first natural prebiotics for newborns, promoting the development of a beneficial gut microbiota. The ability of bacteria to use these complex sugars depends on their structure, but data are limited to bacteria isolated from newborn hum...
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2025-08-01
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| Online Access: | https://doi.org/10.1186/s12866-025-04205-y |
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| author | Mathilde Rumeau Sead Chadi Frederic Pepke Martin Beaumont Cláudia M. Vicente Agathe Juppeau Céline Vandecasteele Laurent Cauquil Géraldine Pascal Philippe Langella Christelle Knudsen Sylvie Combes Rebeca Martín |
| author_facet | Mathilde Rumeau Sead Chadi Frederic Pepke Martin Beaumont Cláudia M. Vicente Agathe Juppeau Céline Vandecasteele Laurent Cauquil Géraldine Pascal Philippe Langella Christelle Knudsen Sylvie Combes Rebeca Martín |
| author_sort | Mathilde Rumeau |
| collection | DOAJ |
| description | Abstract Background Mammalian milk oligosaccharides serve as the first natural prebiotics for newborns, promoting the development of a beneficial gut microbiota. The ability of bacteria to use these complex sugars depends on their structure, but data are limited to bacteria isolated from newborn humans. This study aims to investigate in vitro the functional relationship between the structural variability of milk oligosaccharides and the metabolic capacities of newly intestinal commensal bacteria isolated from suckling rabbits and piglets. Results A total of 240 anaerobic intestinal bacterial strains were isolated from suckling piglets and rabbits, and 9 strains were cultivated in the presence of structurally different milk oligosaccharides: lacto-N-tetraose, 2’-fucosyllactose, and 3’-sialyllactose or 6’-sialyllactose. Five strains, belonging to Bacteroides fragilis, Bacteroides thetaiotaomicron, Bacteroides sp. D2, Bacteroides sp. 3_1_33FAA and Phocaeicola vulgatus were able to utilize milk oligosaccharides. Growth curves revealed that glucose supported faster growth, while, leading to a lower final biomass compared to milk oligosaccharides. Both the growth rate and the final bacterial biomass varied depending on the milk oligosaccharide structure, with higher final biomass reached with 2’-fucosyllactose. The consumption rates of milk oligosaccharides exceeded 40% for all oligosaccharides in B. fragilis, Bacteroides sp. 3_1_33FAA and P. vulgatus strains. Conversely, B. thetaiotaomicron with 6’-sialyllactose and Bacteroides sp. D2 strains for each milk oligosaccharide displayed a consumption rate below 40%. Milk oligosaccharide fermentation generated a more diverse metabolome compared to glucose. Utilization of milk oligosaccharides increased the production of propionate, isobutyrate, isovalerate, 2-methylbutyrate and 1,2-propanediol. Remarkably, fermentation of 2’-fucosyllactose resulted in substantial 1,2-propanediol production. Whole genome sequencing of the bacterial strains revealed the presence of diverse glycoside hydrolase in the strains capable of metabolizing milk oligosaccharides. Conclusions This study demonstrates the capacity of diverse intestinal commensal bacteria from suckling rabbits and piglets to ferment diverse milk oligosaccharide structures, revealing species-specific and milk oligosaccharide structure-dependent metabolization profiles. These findings highlight the potential application of milk oligosaccharides as prebiotic supplements to support gut health in farm animals. |
| format | Article |
| id | doaj-art-5815c6dcead84b348160ef5fcd5aef52 |
| institution | Kabale University |
| issn | 1471-2180 |
| language | English |
| publishDate | 2025-08-01 |
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| series | BMC Microbiology |
| spelling | doaj-art-5815c6dcead84b348160ef5fcd5aef522025-08-20T03:44:00ZengBMCBMC Microbiology1471-21802025-08-0125112410.1186/s12866-025-04205-yStructure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbitsMathilde Rumeau0Sead Chadi1Frederic Pepke2Martin Beaumont3Cláudia M. Vicente4Agathe Juppeau5Céline Vandecasteele6Laurent Cauquil7Géraldine Pascal8Philippe Langella9Christelle Knudsen10Sylvie Combes11Rebeca Martín12GenPhySE, Université de Toulouse, INRAE, ENVTINRAE, AgroParisTech, Micalis Institute, Université Paris-SaclayINRAE, AgroParisTech, Micalis Institute, Université Paris-SaclayGenPhySE, Université de Toulouse, INRAE, ENVTGenPhySE, Université de Toulouse, INRAE, ENVTGenPhySE, Université de Toulouse, INRAE, ENVTGeT-PlaGe, INRAE, Genotoul, France Génomique, Université de ToulouseGenPhySE, Université de Toulouse, INRAE, ENVTGenPhySE, Université de Toulouse, INRAE, ENVTINRAE, AgroParisTech, Micalis Institute, Université Paris-SaclayGenPhySE, Université de Toulouse, INRAE, ENVTGenPhySE, Université de Toulouse, INRAE, ENVTINRAE, AgroParisTech, Micalis Institute, Université Paris-SaclayAbstract Background Mammalian milk oligosaccharides serve as the first natural prebiotics for newborns, promoting the development of a beneficial gut microbiota. The ability of bacteria to use these complex sugars depends on their structure, but data are limited to bacteria isolated from newborn humans. This study aims to investigate in vitro the functional relationship between the structural variability of milk oligosaccharides and the metabolic capacities of newly intestinal commensal bacteria isolated from suckling rabbits and piglets. Results A total of 240 anaerobic intestinal bacterial strains were isolated from suckling piglets and rabbits, and 9 strains were cultivated in the presence of structurally different milk oligosaccharides: lacto-N-tetraose, 2’-fucosyllactose, and 3’-sialyllactose or 6’-sialyllactose. Five strains, belonging to Bacteroides fragilis, Bacteroides thetaiotaomicron, Bacteroides sp. D2, Bacteroides sp. 3_1_33FAA and Phocaeicola vulgatus were able to utilize milk oligosaccharides. Growth curves revealed that glucose supported faster growth, while, leading to a lower final biomass compared to milk oligosaccharides. Both the growth rate and the final bacterial biomass varied depending on the milk oligosaccharide structure, with higher final biomass reached with 2’-fucosyllactose. The consumption rates of milk oligosaccharides exceeded 40% for all oligosaccharides in B. fragilis, Bacteroides sp. 3_1_33FAA and P. vulgatus strains. Conversely, B. thetaiotaomicron with 6’-sialyllactose and Bacteroides sp. D2 strains for each milk oligosaccharide displayed a consumption rate below 40%. Milk oligosaccharide fermentation generated a more diverse metabolome compared to glucose. Utilization of milk oligosaccharides increased the production of propionate, isobutyrate, isovalerate, 2-methylbutyrate and 1,2-propanediol. Remarkably, fermentation of 2’-fucosyllactose resulted in substantial 1,2-propanediol production. Whole genome sequencing of the bacterial strains revealed the presence of diverse glycoside hydrolase in the strains capable of metabolizing milk oligosaccharides. Conclusions This study demonstrates the capacity of diverse intestinal commensal bacteria from suckling rabbits and piglets to ferment diverse milk oligosaccharide structures, revealing species-specific and milk oligosaccharide structure-dependent metabolization profiles. These findings highlight the potential application of milk oligosaccharides as prebiotic supplements to support gut health in farm animals.https://doi.org/10.1186/s12866-025-04205-yMilk oligosaccharidesGut microbiotaBacteroidesGlycoside hydrolaseWhole genome sequencingShort chain fatty acids |
| spellingShingle | Mathilde Rumeau Sead Chadi Frederic Pepke Martin Beaumont Cláudia M. Vicente Agathe Juppeau Céline Vandecasteele Laurent Cauquil Géraldine Pascal Philippe Langella Christelle Knudsen Sylvie Combes Rebeca Martín Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits BMC Microbiology Milk oligosaccharides Gut microbiota Bacteroides Glycoside hydrolase Whole genome sequencing Short chain fatty acids |
| title | Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits |
| title_full | Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits |
| title_fullStr | Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits |
| title_full_unstemmed | Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits |
| title_short | Structure-dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits |
| title_sort | structure dependent degradation of milk oligosaccharides by newly isolated intestinal commensal bacterial strains from suckling piglets and rabbits |
| topic | Milk oligosaccharides Gut microbiota Bacteroides Glycoside hydrolase Whole genome sequencing Short chain fatty acids |
| url | https://doi.org/10.1186/s12866-025-04205-y |
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