Effects of Commercial Apple Varieties on Human Gut Microbiota Composition and Metabolic Output Using an In Vitro Colonic Model

Study information

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-13

study design

laboratory experiment

Citation

PMID PubMed identifier for scientific articles.

28538678

DOI Digital object identifier for electronic documents.

10.3390/nu9060533

URI

Authors

Koutsos A, Lima M, Conterno L, Gasperotti M, Bianchi M, Fava F, Vrhovsek U, Lovegrove JA, Tuohy KM

Journal

Nutrients

Year

2017

Keywords:

Fluorescence in situ hybridization (FISH), Illumina 16S rRNA gene sequencing, apples, fiber, gut microbiota, in vitro batch culture fermentation, microbial metabolites, pectin, polyphenols, proanthocyanidins

Apples are a rich source of polyphenols and fiber. A major proportion of apple polyphenols escape absorption in the small intestine and together with non-digestible polysaccharides reach the colon, where they can serve as substrates for bacterial fermentation. Animal studies suggest a synergistic interaction between apple polyphenols and the soluble fiber pectin; however, the effects of whole apples on human gut microbiota are less extensively studied. Three commercial apple varieties-Renetta Canada, Golden Delicious and Pink Lady-were digested and fermented in vitro using a batch culture colonic model (pH 5.5-6.0, 37 °C) inoculated with feces from three healthy donors. Inulin and cellulose were used as a readily and a poorly fermentable plant fiber, respectively. Fecal microbiota composition was measured by 16S rRNA gene Illumina MiSeq sequencing (V3-V4 region) and Fluorescence in Situ Hybridization. Short chain fatty acids (SCFAs) and polyphenol microbial metabolites were determined. The three apple varieties significantly changed bacterial diversity, increased Actinobacteria relative abundance, acetate, propionate and total SCFAs (p < 0.05). Renetta Canada and Golden Delicious significantly decreased Bacteroidetes abundance and increased Proteobacteria proportion and bifidobacteria population (p < 0.05). Renetta Canada also increased Faecalibacterium prausnitzii, butyrate levels and polyphenol microbial metabolites (p < 0.05). Together, these data suggest that apples, particularly Renetta Canada, can induce substantial changes in microbiota composition and metabolic activity in vitro, which could be associated with potential benefits to human health. Human intervention studies are necessary to confirm these data and potential beneficial effects.

Experiment 1

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Curated date: 2021/01/10

Curator: WikiWorks

Revision editor(s): WikiWorks, ChiomaBlessing

Subjects

Location of subjects

United Kingdom

Host species Species from which microbiome was sampled. Contact us to have more species added.

Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology

Diet Dietary,Diets,Diet,diet

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Poorly fermentable fiber (cellulose)

Group 1 name Corresponds to the case (exposed) group for case-control studies

Renatta canada apple - at 10 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Renetta Canada apple

Group 0 sample size Number of subjects in the control (unexposed) group

3

Group 1 sample size Number of subjects in the case (exposed) group

3

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)

3 months

Lab analysis

Sequencing type

16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene

V3-V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).

relative abundances

Statistical test

ANOVA

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?

Yes

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

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Curated date: 2021/01/10

Curator: Lora Kasselman

Revision editor(s): WikiWorks, ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Renetta Canada apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: decreased abundance in Renatta canada apple - at 10 hr

NCBI	Quality Control	Links
Bilophila
Eubacteriales
Lachnospiraceae
Oscillospira
Parabacteroides
Ruminococcus
unclassified Eubacteriales
unclassified Mogibacterium

Revision editor(s): WikiWorks, ChiomaBlessing

Signature 2

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Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Renetta Canada apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: increased abundance in Renatta canada apple - at 10 hr

NCBI	Quality Control	Links
Bifidobacterium

Revision editor(s): ChiomaBlessing

Experiment 2

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Curated date: 2021/01/10

Curator: WikiWorks

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Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Golden delicious apple - at 10 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Golden delicious apple at 10 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Your review change was submitted

Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-13

Curated date: 2021/01/10

Curator: Lora Kasselman

Revision editor(s): WikiWorks, ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Golden delicious apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: decreased abundance in Golden delicious apple - at 10 hr

NCBI	Quality Control	Links
Eubacteriales
unclassified Mogibacterium
Oscillospira
Ruminococcus
unclassified Eubacteriales
Parabacteroides
Bilophila

Revision editor(s): WikiWorks, ChiomaBlessing

Signature 2

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Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Golden delicious apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: increased abundance in Golden delicious apple - at 10 hr

NCBI	Quality Control	Links
Bifidobacterium

Revision editor(s): ChiomaBlessing

Experiment 3

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Curated date: 2021/01/10

Curator: WikiWorks

Revision editor(s): WikiWorks, ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Pink lady apple - at 10 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Pink lady apple at 10 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-13

Curated date: 2021/01/10

Curator: Lora Kasselman

Revision editor(s): WikiWorks, ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Pink lady apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: decreased abundance in Pink lady apple - at 10 hr

NCBI	Quality Control	Links
Eubacteriales
unclassified Mogibacterium
Lachnospiraceae
Oscillospira
Ruminococcus
unclassified Eubacteriales
Parabacteroides
Bilophila

Revision editor(s): WikiWorks, ChiomaBlessing

Experiment 4

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Curated date: 2024/02/20

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Renetta Canada apple- at 24 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Renetta Canada apple at 24 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Your review change was submitted

Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-20

Curated date: 2024/02/20

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Renetta Canada apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: decreased abundance in Renetta Canada apple- at 24 hr

NCBI	Quality Control	Links
Butyricimonas
Eubacteriales

Revision editor(s): ChiomaBlessing

Signature 2

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Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Renetta Canada apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: increased abundance in Renetta Canada apple- at 24 hr

NCBI	Quality Control	Links
Faecalibacterium
Bifidobacterium

Revision editor(s): ChiomaBlessing

Experiment 5

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Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Golden delicious apple- at 24 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Golden delicious apple at 24 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Your review change was submitted

Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-20

Curated date: 2024/02/20

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Golden delicious apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: decreased abundance in Golden delicious apple- at 24 hr

NCBI	Quality Control	Links
Butyricimonas
Eubacteriales

Revision editor(s): ChiomaBlessing

Signature 2

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-20

Curated date: 2024/02/20

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Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Golden delicious apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: increased abundance in Golden delicious apple- at 24 hr

NCBI	Quality Control	Links
Bifidobacterium

Revision editor(s): ChiomaBlessing

Experiment 6

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-20

Curated date: 2024/02/20

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Pink lady apple- at 24 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Pink lady apple at 24 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-20

Curated date: 2024/02/20

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Pink lady apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: decreased abundance in Pink lady apple- at 24 hr

NCBI	Quality Control	Links
Eubacteriales
Butyricimonas

Revision editor(s): ChiomaBlessing

Signature 2

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-20

Curated date: 2024/02/20

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Pink lady apple compared to those administered with poorly fermentable fiber (cellulose)

Abundance in Group 1: increased abundance in Pink lady apple- at 24 hr

NCBI	Quality Control	Links
Faecalibacterium

Revision editor(s): ChiomaBlessing

Experiment 7

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Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Inulin

Group 1 name Corresponds to the case (exposed) group for case-control studies

Renatta canada apple - at 10 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Renatta canada apple - at 10 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

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Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Renatta canada apple compared to those administered with inulin

Abundance in Group 1: decreased abundance in Renatta canada apple - at 10 hr

NCBI	Quality Control	Links
Eubacteriales
Oscillospira
unclassified Mogibacterium

Revision editor(s): ChiomaBlessing

Signature 2

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Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Renatta canada apple compared to those administered with inulin

Abundance in Group 1: increased abundance in Renatta canada apple - at 10 hr

NCBI	Quality Control	Links
Bifidobacterium

Revision editor(s): ChiomaBlessing

Experiment 8

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Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Golden delicious apple - at 10 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Golden delicious apple - at 10 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Golden delicious apple compared to those administered with inulin

Abundance in Group 1: decreased abundance in Golden delicious apple - at 10 hr

NCBI	Quality Control	Links
unclassified Mogibacterium
Oscillospira
Eubacteriales

Revision editor(s): ChiomaBlessing

Signature 2

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Golden delicious apple compared to those administered with inulin

Abundance in Group 1: decreased abundance in Golden delicious apple - at 10 hr

NCBI	Quality Control	Links
Bifidobacterium

Revision editor(s): ChiomaBlessing

Experiment 9

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Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Golden delicious apple - at 24 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Golden delicious apple - at 24 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Golden delicious apple compared to those administered with inulin

Abundance in Group 1: increased abundance in Golden delicious apple - at 24 hr

NCBI	Quality Control	Links
Faecalibacterium

Revision editor(s): ChiomaBlessing

Experiment 10

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Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Pink Lady apple - at 10 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Pink Lady apple at 10 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with Pink lady apple compared to those administered with inulin

Abundance in Group 1: decreased abundance in Pink Lady apple - at 10 hr

NCBI	Quality Control	Links
unclassified Mogibacterium
Oscillospira
Eubacteriales

Revision editor(s): ChiomaBlessing

Experiment 11

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-21

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Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Pink Lady apple - at 24 hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Healthy donors administered with Pink Lady apple at 24 hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Chao1 Abundance-based estimator of species richness

decreased

Richness Number of species

decreased

Signature 1

EditHistoryDelete

Flag for review

Your review change was submitted

Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with Pink lady apple compared to those administered with inulin

Abundance in Group 1: decreased abundance in Pink Lady apple - at 24 hr

NCBI	Quality Control	Links
Faecalibacterium

Revision editor(s): ChiomaBlessing

Experiment 12

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Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Cellulose - at 10hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Donors administered with cellulose at 10hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Chao1 Abundance-based estimator of species richness

increased

Richness Number of species

increased

Signature 1

EditHistoryDelete

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 10 h in donors administered with cellulose compared to those administered with inulin

Abundance in Group 1: increased abundance in Cellulose - at 10hr

NCBI	Quality Control	Links
Bilophila
Eubacteriales
Lachnospiraceae
Oscillospira
Parabacteroides
unclassified Eubacteriales

Revision editor(s): ChiomaBlessing

Experiment 13

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/21

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies

Cellulose - at 24hr

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Donors administered with cellulose at 24hr

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Chao1 Abundance-based estimator of species richness

increased

Richness Number of species

increased

Signature 1

EditHistoryDelete

Flag for review

Your review change was submitted

Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with cellulose compared to those administered with inulin

Abundance in Group 1: decreased abundance in Cellulose - at 24hr

NCBI	Quality Control	Links
Faecalibacterium

Revision editor(s): ChiomaBlessing

Signature 2

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Reviewed Marked as Reviewed by ChiomaBlessing on 2024-2-26

Curated date: 2024/02/26

Curator: ChiomaBlessing

Revision editor(s): ChiomaBlessing

Source: Table 2

Description: Changes in bacterial taxa relative abundance (%) at 24 h in donors administered with cellulose compared to those administered with inulin

Abundance in Group 1: increased abundance in Cellulose - at 24hr

NCBI	Quality Control	Links
Eubacteriales

Revision editor(s): ChiomaBlessing