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Glycan cross-feeding activities between bifidobacteria under in vitro conditions.

Turroni F, Özcan E, Milani C, Mancabelli L, Viappiani A, van Sinderen D, Sela DA, Ventura M - Front Microbiol (2015)

Bottom Line: The glycan-associated metabolic features encoded by bifidobacteria are believed to be strongly influenced by cross-feeding activities due to the co-existence of strains with different glycan-degrading properties.This enhanced growth phenomenon was confirmed by whole genome transcriptome analyses, which revealed co-cultivation-associated transcriptional induction of PRL2010 genes involved in carbohydrate metabolism, such as those encoding for carbohydrate transporters and associated energy production, and genes required for translation, ribosomal structure, and biogenesis, thus supporting the idea that co-cultivation of certain bifidobacterial strains with B. bifidum PRL2010 causes enhanced metabolic activity, and consequently increased lactate and/or acetate production.Overall, these data suggest that PRL2010 cells benefit from the presence of other bifidobacterial strains.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Probiogenomics, Department of Life Sciences, University of Parma, Parma Italy.

ABSTRACT
Bifidobacteria colonize the gut of various mammals, including humans, where they may metabolize complex, diet-, and host-derived carbohydrates. The glycan-associated metabolic features encoded by bifidobacteria are believed to be strongly influenced by cross-feeding activities due to the co-existence of strains with different glycan-degrading properties. In this study, we observed an enhanced growth yield of Bifidobacterium bifidum PRL2010 when co-cultivated with Bifidobacterium breve 12L, Bifidobacterium adolescentis 22L, or Bifidobacterium thermophilum JCM1207. This enhanced growth phenomenon was confirmed by whole genome transcriptome analyses, which revealed co-cultivation-associated transcriptional induction of PRL2010 genes involved in carbohydrate metabolism, such as those encoding for carbohydrate transporters and associated energy production, and genes required for translation, ribosomal structure, and biogenesis, thus supporting the idea that co-cultivation of certain bifidobacterial strains with B. bifidum PRL2010 causes enhanced metabolic activity, and consequently increased lactate and/or acetate production. Overall, these data suggest that PRL2010 cells benefit from the presence of other bifidobacterial strains.

No MeSH data available.


Related in: MedlinePlus

Transcriptome analyses of co-cultivated bifidobacterial strains. Only bi-associations showing a cross-feeding behavior between bifidobacterial strains are represented. (A–D) The cell number evaluation of Bifidobacterium breve 12L, Bifidobacterium bifidum PRL2010, Bifidobacterium adolescentis 22L, and Bifidobacterium thermophilum JCM1207 strains in mono- and co-cultivation on the glycans-based medium indicated above each panel by qRT-PCR. The bar plot placed below represented the functional annotation of expressed genes of bi-association according to their cluster orthologous gene (COG) categories. Results of qRT-PCR are represented in pillars in which the y-axis represents the genome copy number/ml of bacterial culture and x-axis showed the name of the strains involved in mono- and bi-associations. The value in parenthesis above each pillar represents the average cell numbers for that condition. The color of each COG family is indicated in the figure. Each COG family is identified by one-letter abbreviations: A, RNA processing and modification; B, chromatin structure and dynamics; C, energy production and conversion; D, cell cycle control and mitosis; E, amino acid metabolism and transport; F, nucleotide metabolism and transport; G, carbohydrate metabolism and transport; H, coenzyme metabolism; I, lipid metabolism; J, translation; K, transcription; L, replication and repair; M, cell wall/membrane/envelop biogenesis; N, cell motility; O, post-translational modification, protein turnover, chaperone functions; P, inorganic ion transport and metabolism; Q, secondary structure; T, signal transduction; U, intracellular trafficking and secretion; Y, nuclear structure; Z, cytoskeleton; R, general functional prediction only; S, function unknown. The percentage was calculated as the percentage of transcribed genes belonging to the indicated COG category with respect to all transcribed genes. Asterisks indicate that the presented data display a significant, either ∗p < 0.05 or ∗∗p < 0.01, deviation from the obtained values of the mono-association.
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Figure 1: Transcriptome analyses of co-cultivated bifidobacterial strains. Only bi-associations showing a cross-feeding behavior between bifidobacterial strains are represented. (A–D) The cell number evaluation of Bifidobacterium breve 12L, Bifidobacterium bifidum PRL2010, Bifidobacterium adolescentis 22L, and Bifidobacterium thermophilum JCM1207 strains in mono- and co-cultivation on the glycans-based medium indicated above each panel by qRT-PCR. The bar plot placed below represented the functional annotation of expressed genes of bi-association according to their cluster orthologous gene (COG) categories. Results of qRT-PCR are represented in pillars in which the y-axis represents the genome copy number/ml of bacterial culture and x-axis showed the name of the strains involved in mono- and bi-associations. The value in parenthesis above each pillar represents the average cell numbers for that condition. The color of each COG family is indicated in the figure. Each COG family is identified by one-letter abbreviations: A, RNA processing and modification; B, chromatin structure and dynamics; C, energy production and conversion; D, cell cycle control and mitosis; E, amino acid metabolism and transport; F, nucleotide metabolism and transport; G, carbohydrate metabolism and transport; H, coenzyme metabolism; I, lipid metabolism; J, translation; K, transcription; L, replication and repair; M, cell wall/membrane/envelop biogenesis; N, cell motility; O, post-translational modification, protein turnover, chaperone functions; P, inorganic ion transport and metabolism; Q, secondary structure; T, signal transduction; U, intracellular trafficking and secretion; Y, nuclear structure; Z, cytoskeleton; R, general functional prediction only; S, function unknown. The percentage was calculated as the percentage of transcribed genes belonging to the indicated COG category with respect to all transcribed genes. Asterisks indicate that the presented data display a significant, either ∗p < 0.05 or ∗∗p < 0.01, deviation from the obtained values of the mono-association.

Mentions: Growth capabilities of B. bifidum PRL2010, B. adolescentis 22L, B. breve 12L, and B. thermophilum JCM1207 cultivated on their own (mono-association) on MRS supplemented with starch or xylan as the sole carbon source were evaluated (Figure 1; Supplementary Figure S1) and compared to those achieved when these strains were co-cultivated in pairs (bi-associations) on identical substrates. In addition, cultivation experiments involving all the strains used in this study were also performed on MRS without carbon source, revealing, as expected, the absence of any sign of growth. These carbohydrates were selected in order to represent carbon sources that may occur in the human gut as they are derived from a plant-derived, glycan-based diet (Chassard and Lacroix, 2013). Notably, of all the possible strain pair combinations, only those bi-associations that included PRL2010 cells displayed significant differences in growth with respect to the respective mono-associations (Figure 1; Supplementary Figure S1). As expected, PRL2010 cells did not exhibit any significant growth on starch or xylan when grown in a mono-culture (Turroni et al., 2012). However, when this strain was co-cultivated with 22L or 12L cells on a MRS-supplemented with starch, the number of cells increased (about three- and fourfold, respectively, p < 0.005) compared to the situation of mono-association, respectively (Figure 1). In contrast, 12L appears to significant decrease (compared to mono-association; fourfold, p < 0.001) during growth on starch when co-cultivated with the presence of PRL2010 cells (Figure 1). Conversely, B. bifidum PRL2010 did not appear to influence the growth yields (changes less than twofold) of 22L cells on starch, or that of 12L when cultivated on xylan, as displayed by unchanged growth yields of bi-association compared to mono-association of these strains (Figure 1). Another interesting increase in deduced PRL2010 cell numbers was observed for the bi-association of PRL2010 with B. thermophilum JCM1207 (threefold, p < 0.001), when grown on MRS supplemented with xylan (Figure 1). In contrast, JCM1207 cells exhibit a modest reduction in growth ability (relative to mono-association), when co-cultivated with PRL2010 (Figure 1; Supplementary Figure S1). Overall, the concomitant presence of two different bifidobacterial strains was shown in some cases to increase the cell numbers of one partner when cultivated on complex carbohydrates, thus suggesting cross-feeding abilities of bifidobacterial strains.


Glycan cross-feeding activities between bifidobacteria under in vitro conditions.

Turroni F, Özcan E, Milani C, Mancabelli L, Viappiani A, van Sinderen D, Sela DA, Ventura M - Front Microbiol (2015)

Transcriptome analyses of co-cultivated bifidobacterial strains. Only bi-associations showing a cross-feeding behavior between bifidobacterial strains are represented. (A–D) The cell number evaluation of Bifidobacterium breve 12L, Bifidobacterium bifidum PRL2010, Bifidobacterium adolescentis 22L, and Bifidobacterium thermophilum JCM1207 strains in mono- and co-cultivation on the glycans-based medium indicated above each panel by qRT-PCR. The bar plot placed below represented the functional annotation of expressed genes of bi-association according to their cluster orthologous gene (COG) categories. Results of qRT-PCR are represented in pillars in which the y-axis represents the genome copy number/ml of bacterial culture and x-axis showed the name of the strains involved in mono- and bi-associations. The value in parenthesis above each pillar represents the average cell numbers for that condition. The color of each COG family is indicated in the figure. Each COG family is identified by one-letter abbreviations: A, RNA processing and modification; B, chromatin structure and dynamics; C, energy production and conversion; D, cell cycle control and mitosis; E, amino acid metabolism and transport; F, nucleotide metabolism and transport; G, carbohydrate metabolism and transport; H, coenzyme metabolism; I, lipid metabolism; J, translation; K, transcription; L, replication and repair; M, cell wall/membrane/envelop biogenesis; N, cell motility; O, post-translational modification, protein turnover, chaperone functions; P, inorganic ion transport and metabolism; Q, secondary structure; T, signal transduction; U, intracellular trafficking and secretion; Y, nuclear structure; Z, cytoskeleton; R, general functional prediction only; S, function unknown. The percentage was calculated as the percentage of transcribed genes belonging to the indicated COG category with respect to all transcribed genes. Asterisks indicate that the presented data display a significant, either ∗p < 0.05 or ∗∗p < 0.01, deviation from the obtained values of the mono-association.
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Figure 1: Transcriptome analyses of co-cultivated bifidobacterial strains. Only bi-associations showing a cross-feeding behavior between bifidobacterial strains are represented. (A–D) The cell number evaluation of Bifidobacterium breve 12L, Bifidobacterium bifidum PRL2010, Bifidobacterium adolescentis 22L, and Bifidobacterium thermophilum JCM1207 strains in mono- and co-cultivation on the glycans-based medium indicated above each panel by qRT-PCR. The bar plot placed below represented the functional annotation of expressed genes of bi-association according to their cluster orthologous gene (COG) categories. Results of qRT-PCR are represented in pillars in which the y-axis represents the genome copy number/ml of bacterial culture and x-axis showed the name of the strains involved in mono- and bi-associations. The value in parenthesis above each pillar represents the average cell numbers for that condition. The color of each COG family is indicated in the figure. Each COG family is identified by one-letter abbreviations: A, RNA processing and modification; B, chromatin structure and dynamics; C, energy production and conversion; D, cell cycle control and mitosis; E, amino acid metabolism and transport; F, nucleotide metabolism and transport; G, carbohydrate metabolism and transport; H, coenzyme metabolism; I, lipid metabolism; J, translation; K, transcription; L, replication and repair; M, cell wall/membrane/envelop biogenesis; N, cell motility; O, post-translational modification, protein turnover, chaperone functions; P, inorganic ion transport and metabolism; Q, secondary structure; T, signal transduction; U, intracellular trafficking and secretion; Y, nuclear structure; Z, cytoskeleton; R, general functional prediction only; S, function unknown. The percentage was calculated as the percentage of transcribed genes belonging to the indicated COG category with respect to all transcribed genes. Asterisks indicate that the presented data display a significant, either ∗p < 0.05 or ∗∗p < 0.01, deviation from the obtained values of the mono-association.
Mentions: Growth capabilities of B. bifidum PRL2010, B. adolescentis 22L, B. breve 12L, and B. thermophilum JCM1207 cultivated on their own (mono-association) on MRS supplemented with starch or xylan as the sole carbon source were evaluated (Figure 1; Supplementary Figure S1) and compared to those achieved when these strains were co-cultivated in pairs (bi-associations) on identical substrates. In addition, cultivation experiments involving all the strains used in this study were also performed on MRS without carbon source, revealing, as expected, the absence of any sign of growth. These carbohydrates were selected in order to represent carbon sources that may occur in the human gut as they are derived from a plant-derived, glycan-based diet (Chassard and Lacroix, 2013). Notably, of all the possible strain pair combinations, only those bi-associations that included PRL2010 cells displayed significant differences in growth with respect to the respective mono-associations (Figure 1; Supplementary Figure S1). As expected, PRL2010 cells did not exhibit any significant growth on starch or xylan when grown in a mono-culture (Turroni et al., 2012). However, when this strain was co-cultivated with 22L or 12L cells on a MRS-supplemented with starch, the number of cells increased (about three- and fourfold, respectively, p < 0.005) compared to the situation of mono-association, respectively (Figure 1). In contrast, 12L appears to significant decrease (compared to mono-association; fourfold, p < 0.001) during growth on starch when co-cultivated with the presence of PRL2010 cells (Figure 1). Conversely, B. bifidum PRL2010 did not appear to influence the growth yields (changes less than twofold) of 22L cells on starch, or that of 12L when cultivated on xylan, as displayed by unchanged growth yields of bi-association compared to mono-association of these strains (Figure 1). Another interesting increase in deduced PRL2010 cell numbers was observed for the bi-association of PRL2010 with B. thermophilum JCM1207 (threefold, p < 0.001), when grown on MRS supplemented with xylan (Figure 1). In contrast, JCM1207 cells exhibit a modest reduction in growth ability (relative to mono-association), when co-cultivated with PRL2010 (Figure 1; Supplementary Figure S1). Overall, the concomitant presence of two different bifidobacterial strains was shown in some cases to increase the cell numbers of one partner when cultivated on complex carbohydrates, thus suggesting cross-feeding abilities of bifidobacterial strains.

Bottom Line: The glycan-associated metabolic features encoded by bifidobacteria are believed to be strongly influenced by cross-feeding activities due to the co-existence of strains with different glycan-degrading properties.This enhanced growth phenomenon was confirmed by whole genome transcriptome analyses, which revealed co-cultivation-associated transcriptional induction of PRL2010 genes involved in carbohydrate metabolism, such as those encoding for carbohydrate transporters and associated energy production, and genes required for translation, ribosomal structure, and biogenesis, thus supporting the idea that co-cultivation of certain bifidobacterial strains with B. bifidum PRL2010 causes enhanced metabolic activity, and consequently increased lactate and/or acetate production.Overall, these data suggest that PRL2010 cells benefit from the presence of other bifidobacterial strains.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Probiogenomics, Department of Life Sciences, University of Parma, Parma Italy.

ABSTRACT
Bifidobacteria colonize the gut of various mammals, including humans, where they may metabolize complex, diet-, and host-derived carbohydrates. The glycan-associated metabolic features encoded by bifidobacteria are believed to be strongly influenced by cross-feeding activities due to the co-existence of strains with different glycan-degrading properties. In this study, we observed an enhanced growth yield of Bifidobacterium bifidum PRL2010 when co-cultivated with Bifidobacterium breve 12L, Bifidobacterium adolescentis 22L, or Bifidobacterium thermophilum JCM1207. This enhanced growth phenomenon was confirmed by whole genome transcriptome analyses, which revealed co-cultivation-associated transcriptional induction of PRL2010 genes involved in carbohydrate metabolism, such as those encoding for carbohydrate transporters and associated energy production, and genes required for translation, ribosomal structure, and biogenesis, thus supporting the idea that co-cultivation of certain bifidobacterial strains with B. bifidum PRL2010 causes enhanced metabolic activity, and consequently increased lactate and/or acetate production. Overall, these data suggest that PRL2010 cells benefit from the presence of other bifidobacterial strains.

No MeSH data available.


Related in: MedlinePlus