Gut microbiota affects the estrus return of sows by regulating the metabolism of sex steroid hormones

From BugSigDB
Reviewed Marked as Reviewed by KateRasheed on 2025-6-11
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI Uniform resource identifier for web resources.
Authors
Liu M, Zhang J, Zhou Y, Xiong S, Zhou M, Wu L, Liu Q, Chen Z, Jiang H, Yang J, Liu Y, Wang Y, Chen C, Huang L
Journal
Journal of animal science and biotechnology
Year
2023
Keywords:
Estrus return, Fecal metabolome, Gut microbiota, Metagenomics, Sex steroid hormones, Sow
BACKGROUND: Sex hormones play important roles in the estrus return of post-weaning sows. Previous studies have demonstrated a complex and bi-directional regulation between sex hormones and gut microbiota. However, the extent to which the gut microbiota affects estrus return of post-weaning sows is largely unknown. RESULTS: In this study, we first screened 207 fecal samples from well-phenotyped sows by 16S rRNA gene sequencing and identified significant associations between microbes and estrus return of post-weaning sows. Using metagenomic sequencing data from 85 fecal samples, we identified 37 bacterial species that were significantly associated with estrus return. Normally returning sows were characterized by increased abundances of L. reuteri and P. copri and decreased abundances of B. fragilis, S. suis, and B. pseudolongum. The changes in gut microbial composition significantly altered the functional capacity of steroid hormone biosynthesis in the gut microbiome. The results were confirmed in a validation cohort. Significant changes in sex steroid hormones and related compounds were found between normal and non-return sows via metabolome analysis. An integrated analysis of differential bacterial species, metagenome, and fecal metabolome provided evidence that normal return-associated bacterial species L. reuteri and Prevotella spp. participated in the degradation of pregnenolone, progesterone, and testosterone, thereby promoting estrogen biosynthesis. Furthermore, the microbial metabolites related to sow energy and nutrient supply or metabolic disorders also showed relationships with sow estrus return. CONCLUSIONS: An integrated analysis of differentially abundant bacterial species, metagenome, and fecal metabolome revealed the involvement of L. reuteri and Prevotella spp. in sow estrus return. These findings provide deep insight into the role of gut microbiota in the estrus return of post-weaning sows and the complex cross-talk between gut microbiota and sex hormones, suggesting that the manipulation of the gut microbiota could be an effective strategy to improve sow estrus return after weaning.

Experiment 1


Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/04/25

Curator: Victoria

Revision editor(s): Victoria

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled. Contact us to have more species added.
Sus scrofa domesticus
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
Sex hormone Geschlechtshormon,Geschlechtshormone,hormone sexuelle,hormones sexuelles,sex hormones,Sexualhormon,Sexualhormone,Sex hormone,sex hormone
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-return sows (Discovery cohort)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Normal Return sows (Discovery cohort)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
This group comprises sows that returned to estrus within 7 days of weaning in the discovery cohort.
Group 0 sample size Number of subjects in the control (unexposed) group
40
Group 1 sample size Number of subjects in the case (exposed) group
45

Lab analysis

Sequencing type
WMS
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
Not specified
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
LEfSe
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)?
No
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
decreased
Richness Number of species
decreased

Signature 1

Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/04/25

Curator: Victoria

Revision editor(s): Victoria

Source: Figure 1D, Additional file1: Figure S5D & Additional file 2: Table S4

Description: Differential bacterial species between normal return and non-return sows in 85 faecal samples with metagenomic sequencing data.

Abundance in Group 1: increased abundance in Normal Return sows (Discovery cohort)

NCBI Quality ControlLinks
Bacillota
Bacteroidales
Bacteroides
Bacteroides ovatus
Bacteroidota
Fibrobacter
Hallerella succinigenes
Lachnospiraceae bacterium
Lactobacillus gasseri
Lactobacillus johnsonii
Limosilactobacillus reuteri
Methanobrevibacter
Methanobrevibacter olleyae
Muribaculaceae
Parabacteroides goldsteinii
Prevotella
Prevotella disiens
Prevotella intermedia
Prevotella sp. P2-180
Prevotella sp. P3-122
Prevotella sp. P5-92
Prevotellaceae
Segatella bryantii
Segatella copri
Treponema sp.
Verrucomicrobiota bacterium
Xylanibacter ruminicola
Candidatus Alcium sp. P201
unclassified Bacillota
unclassified Muribaculaceae
uncultured Dysgonomonas sp.

Revision editor(s): Victoria

Signature 2

Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/04/25

Curator: Victoria

Revision editor(s): Victoria

Source: Figure 1D, Additional file1: Figure S5D & Additional file 2: Table S4

Description: Differential bacterial species between normal return and non-return sows in 85 faecal samples with metagenomic sequencing data.

Abundance in Group 1: decreased abundance in Normal Return sows (Discovery cohort)

NCBI Quality ControlLinks
Bacteroides fragilis
Bifidobacterium
Bifidobacterium pseudolongum
Citrobacter amalonaticus
Corynebacterium xerosis
Enterococcus
Enterococcus cecorum
Enterococcus faecalis
Enterococcus faecium
Felixounavirus
Lactobacillales
Lactococcus
Lactococcus lactis
Methanobrevibacter smithii
Pediococcus pentosaceus
Phocaeicola plebeius
Streptococcaceae
Streptococcus
Streptococcus equinus
Streptococcus gallolyticus
Streptococcus pneumoniae
Streptococcus suis
Streptococcus thermophilus
Thomasclavelia ramosa

Revision editor(s): Victoria

Experiment 2


Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/04/25

Curator: Victoria

Revision editor(s): Victoria

Differences from previous experiment shown

Subjects

Group 1 sample size Number of subjects in the case (exposed) group
167

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V3-V4

Statistical Analysis

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
3

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/04/25

Curator: Victoria

Revision editor(s): Victoria

Source: Additional file 1: Figure S4 D&E, Additional file2: Table S2

Description: Differential ASVs and genera between normal return and non-return sows in 207 fecal samples.

Abundance in Group 1: increased abundance in Normal Return sows (Discovery cohort)

NCBI Quality ControlLinks
Bacteroidales
Lactobacillus johnsonii
Muribaculaceae
Prevotella
Ruminococcaceae bacterium UCG-005
Candidatus Alcium sp. F082
uncultured eubacterium WCHB1-41
Bacteroidales RF16 groupBacteroidales RF16 group
Rikenellaceae RC9 gut groupRikenellaceae RC9 gut group
Lachnospiraceae XPB1014 groupLachnospiraceae XPB1014 group
Prevotellaceae UCG-003Prevotellaceae UCG-003

Revision editor(s): Victoria

Signature 2

Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/04/25

Curator: Victoria

Revision editor(s): Victoria, KateRasheed

Source: Additional file 1: Figure S4 D&E, Additional file2: Table S2

Description: Differential ASVs and genera between normal return and non-return sows in 207 fecal samples.

Abundance in Group 1: decreased abundance in Normal Return sows (Discovery cohort)

NCBI Quality ControlLinks
Bacteroides
Bacteroides fragilis
Bifidobacterium
Bifidobacterium pseudolongum
Cellulosilyticum
Clostridium
Clostridium bornimense
Clostridium perfringens
Clostridium septicum
Enterococcus
Eubacterium coprostanoligenes
Lachnospiraceae
Lachnospiraceae bacterium XBB1006
Mogibacterium sp.
Negativibacillus
Oscillospiraceae
Parabacteroides
Peptococcaceae
Phocaeicola plebeius
Streptococcus
Terrisporobacter
Rikenellaceae RC9 gut groupRikenellaceae RC9 gut group
Christensenellaceae R-7 groupChristensenellaceae R-7 group
Clostridia UCG-014Clostridia UCG-014
NK4A214 groupNK4A214 group
Family XIII AD3011 groupFamily XIII AD3011 group
Clostridium sensu stricto 6Clostridium sensu stricto 6
Ruminococcaceae bacterium UCG-005

Revision editor(s): Victoria, KateRasheed

Experiment 3


Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/05/11

Curator: Victoria

Revision editor(s): Victoria

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-return Sows (Validation cohort)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Normal Return Sows (Validation cohort)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
This group comprises sows that returned to estrus within 7 days of weaning in the validation cohort.
Group 0 sample size Number of subjects in the control (unexposed) group
11
Group 1 sample size Number of subjects in the case (exposed) group
18

Lab analysis

Sequencing type
WMS
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
Not specified

Statistical Analysis

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.1
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
No
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/05/11

Curator: Victoria

Revision editor(s): Victoria

Source: Additional file1: Figure S6D

Description: Differential bacterial species between normal return and non-return sows with metagenomic sequencing data in the validation cohort.

Abundance in Group 1: increased abundance in Normal Return Sows (Validation cohort)

NCBI Quality ControlLinks
Lactobacillus johnsonii
Rikenellaceae bacterium
Lactobacillus delbrueckii
Lactobacillus crispatus
Verrucomicrobiota bacterium
Lactobacillus gasseri
Porphyromonadaceae bacterium
Lactobacillus helveticus
Limosilactobacillus fermentum
Lactobacillus taiwanensis
Jonquetella anthropi

Revision editor(s): Victoria

Signature 2

Reviewed Marked as Reviewed by KateRasheed on 2025-6-11

Curated date: 2025/05/11

Curator: Victoria

Revision editor(s): Victoria

Source: Additional file1: Figure S6D

Description: Differential bacterial species between normal return and non-return sows with metagenomic sequencing data in the validation cohort.

Abundance in Group 1: decreased abundance in Normal Return Sows (Validation cohort)

NCBI Quality ControlLinks
[Eubacterium] siraeum
Bifidobacterium pseudolongum
Streptococcus suis
[Ruminococcus] lactaris
Streptococcus equinus
Collinsella aerofaciens
bacterium D16-59
Criibacterium bergeronii
Psychrobacter piechaudii
Bacteroidales bacterium
Bacteroides faecis
Clostridium tertium
Anaerobutyricum hallii
Aerococcus viridans
Streptococcus constellatus
Synergistes jonesii

Revision editor(s): Victoria