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Metagenomic analysis unravels novel taxonomic differences in the uterine microbiome between healthy mares and mares with endometritis.
Abstract: The application of high throughput technologies has enabled unravelling of unique differences between healthy mares and mares with endometritis at transcriptomic and proteomic levels. However, differences in the uterine microbiome are yet to be investigated. Objective: The present study was aimed at evaluating the differences in uterine microbiome between healthy mares and mares with endometritis. Methods: Low-volume lavage (LVL) samples were collected from the uterus of 30 mares classified into healthy (n = 15) and endometritis (n = 15) based on their reproductive history, intrauterine fluid accumulation, gross appearance of LVL samples, endometrial cytology and bacterial culture. The samples were subjected to 16S rRNA sequencing. Results: Notable differences in the uterine microbiome were observed between healthy mares and mares with endometritis at various taxonomic levels. In healthy mares, the most abundant phylum, class, order and family were Firmicutes, Bacilli, Bacillales and Paenibacillaceae, respectively. In contrast, the most abundant corresponding taxonomic levels in mares with endometritis were Proteobacteria, Gammaproteobacteria, Enterobacterales and Enterobacteriaceae, respectively. At the genus level, Brevibacillus and Paenibacillus were more abundant in healthy mares, whereas Escherichia, Salmonella and Klebsiella were more abundant in mares with endometritis. In healthy mares, Brevibacillus brevis was the most abundant species, followed by Brevibacillus choshinensis and Paenibacillus sp JDR-2. However, in mares with endometritis, Escherichia coli was the most abundant species, followed by Salmonella enterica and Klebsiella pneumoniae. Conclusions: These results confirmed the previously reported presence of a uterine microbiome in healthy mares and helped unravel some alterations that occur in mares with endometritis. The findings can potentially help formulate new approaches to prevent or treat equine endometritis.
© 2024 The Authors. Veterinary Medicine and Science published by John Wiley & Sons Ltd.
Publication Date: 2024-02-15 PubMed ID: 38357732PubMed Central: PMC10867593DOI: 10.1002/vms3.1369Google Scholar: Lookup The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
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This research examined the differences in the uterine microbiome between healthy mares and mares suffering from endometritis, an infection of the uterus. The study found specific alterations in the microbiome of diseased mares, providing insights that could lead to new prevention and treatment approaches.
Research Objective and Methodology
- The goal of this study was to determine the differences in the uterine microbiome between healthy horses and those with endometritis, a common uterine infection in mares.
- Using a method known as “low-volume lavage” (essentially a small-scale washing procedure), the researchers collected samples from the uterus of 30 mares, 15 of which were healthy and 15 had endometritis. The classification was based on each mare’s reproductive history, the presence of intrauterine fluid, physical appearance of the sample, and results from cytology and bacterial culture.
- The samples underwent 16S rRNA sequencing, a process used to identify and compare bacteria from the collected samples.
Key Findings
- The study identified distinct differences in the microbiome of healthy mares and mares with endometritis at various taxonomic levels.
- In healthy horses, the microbiome was largely composed of several taxa: the phylum Firmicutes; the class Bacilli; the order Bacillales; and the family Paenibacillaceae.
- In contrast, mares with endometritis saw higher levels of different taxa, including Proteobacteria, Gammaproteobacteria, Enterobacterales, and Enterobacteriaceae.
- At the genus level, the bacteria Brevibacillus and Paenibacillus were predominant in healthy mares, while the bacteria Escherichia, Salmonella, and Klebsiella were more abundant in mares with endometritis.
- The most common bacterial species in healthy mares were Brevibacillus brevis, Brevibacillus choshinensis, and Paenibacillus sp JDR-2. For mares with endometritis, the most prevalent species were Escherichia coli, Salmonella enterica, and Klebsiella pneumoniae.
Conclusions
- The results corroborated previous findings of a uterine microbiome in healthy mares and were able to discern specific changes that occur when a mare has endometritis.
- This newfound understanding of the uterine microbiome changes linked to endometritis could potentially aid in the development of new strategies for prevention and treatment of equine endometritis.
Cite This Article
APA
Virendra A, Gulavane SU, Ahmed ZA, Reddy R, Chaudhari RJ, Gaikwad SM, Shelar RR, Ingole SD, Thorat VD, Khanam A, Khan FA.
(2024).
Metagenomic analysis unravels novel taxonomic differences in the uterine microbiome between healthy mares and mares with endometritis.
Vet Med Sci, 10(2), e1369.
https://doi.org/10.1002/vms3.1369 Publication
Researcher Affiliations
- Department of Animal Reproduction, Gynecology and Obstetrics, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Department of Animal Reproduction, Gynecology and Obstetrics, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Equus Stud Farm, Pune, Maharashtra, India.
- Nanoli Stud and Agricultural Farm, Pune, Maharashtra, India.
- Department of Animal Reproduction, Gynecology and Obstetrics, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Department of Animal Reproduction, Gynecology and Obstetrics, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Department of Animal Reproduction, Gynecology and Obstetrics, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Department of Veterinary Physiology, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Department of Veterinary Microbiology, Mumbai Veterinary College, Mumbai, Maharashtra, India.
- Department of Large Animal Medicine and Surgery, School of Veterinary Medicine, St. George's University, Grenada, West Indies.
- Department of Large Animal Medicine and Surgery, School of Veterinary Medicine, St. George's University, Grenada, West Indies.
MeSH Terms
- Horses
- Animals
- Female
- Endometritis / veterinary
- Proteomics
- RNA, Ribosomal, 16S
- Uterus
- Microbiota
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.
References
This article includes 31 references
- Albihn A, Båverud V, Magnusson U. Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems. Acta Veterinaria Scandinavica 44(3–4), 121–129.
- Ballas P, Reinländer U, Schlegl R, Ehling‐Schulz M, Drillich M, Wagener K. Characterization of intrauterine cultivable aerobic microbiota at the time of insemination in dairy cows with and without mild endometritis. Theriogenology 159, 28–34.
- Bicalho M L S, Lima S, Higgins C H, Machado V S, Lima F S, Bicalho R C. Genetic and functional analysis of the bovine uterine microbiota. Part II: Purulent vaginal discharge versus healthy cows. Journal of Dairy Science 100(5), 3863–3874.
- Clemmons B A, Reese S T, Dantas F G, Franco G A, Smith T P L, Adeyosoye O I, Pohler K G, Myer P R. Vaginal and uterine bacterial communities in postpartum lactating cows. Frontiers in Microbiology 8, 1047.
- Díaz‐Bertrana M L, Deleuze S, Pitti Rios L, Yeste M, Morales Fariña I, Rivera Del Alamo M M. Microbial prevalence and antimicrobial sensitivity in equine endometritis in field conditions. Animals 11(5), 1476.
- Diel de Amorim M, Khan F A, Chenier T S, Scholtz E L, Hayes M A. Analysis of the uterine flush fluid proteome of healthy mares and mares with endometritis or fibrotic endometrial degeneration. Reproduction, Fertility, and Development 32(6), 572–581.
- Durazzi F, Sala C, Castellani G, Manfreda G, Remondini D, De Cesare A. Comparison between 16S rRNA and shotgun sequencing data for the taxonomic characterization of the gut microbiota. Scientific Reports 11(1), 3030.
- Frontoso R, De Carlo E, Pasolini M P, van der Meulen K, Pagnini U, Iovane G, De Martino L. Retrospective study of bacterial isolates and their antimicrobial susceptibilities in equine uteri during fertility problems. Research in Veterinary Science 84(1), 1–6.
- Heil B A, Thompson S K, Kearns T A, Davolli G M, King G, Sones J L. Metagenetic characterization of the resident equine uterine microbiome using multiple techniques. Journal of Equine Veterinary Science 66, 111.
- Holyoak G R, Premathilake H U, Lyman C C, Sones J L, Gunn A, Wieneke X, DeSilva U. The healthy equine uterus harbors a distinct core microbiome plus a rich and diverse microbiome that varies with geographical location. Scientific Reports 12(1), 14790.
- Hurtgen J P. Pathogenesis and treatment of endometritis in the mare: A review. Theriogenology 66(3), 560–566.
- Jianmei C, Bo L, Zheng C, Huai S, Guohong L, Cibin G. Identification of ethylparaben as the antimicrobial substance produced by Brevibacillus brevis FJAT‐0809‐GLX. Microbiological Research 172, 48–56.
- Katila T. Evaluation of diagnostic methods in equine endometritis. Reproductive Biology 16, 189–196.
- Lamoureux C, Surgers L, Fihman V, Gricourt G, Demontant V, Trawinski E, N'Debi M, Gomart C, Royer G, Launay N, Le Glaunec J M, Wemmert C, La Martire G, Rossi G, Lepeule R, Pawlotsky J M, Rodriguez C, Woerther P L. Prospective comparison between shotgun metagenomics and sanger sequencing of the 16S rRNA gene for the etiological diagnosis of infections. Frontiers in Microbiology 13, 761873.
- LeBlanc M M, Causey R C. Clinical and subclinical endometritis in the mare: Both threats to fertility. Reproduction in Domestic Animals = Zuchthygiene 44, 10–22.
- LeBlanc M M, Magsig J, Stromberg A J. Use of a low‐volume uterine flush for diagnosing endometritis in chronically infertile mares. Theriogenology 68(3), 403–412.
- LeBlanc M M. Advances in the diagnosis and treatment of chronic infectious and post‐mating‐induced endometritis in the mare. Reproduction in Domestic Animals = Zuchthygiene 45(Suppl 2), 21–27.
- Lyman C C, Holyoak G R, Meinkoth K, Wieneke X, Chillemi K A, DeSilva U. Canine endometrial and vaginal microbiomes reveal distinct and complex ecosystems. PLoS ONE 14(1), e0210157.
- Maloney S E, Khan F A, Chenier T S, Diel de Amorim M, Anthony Hayes M, Scholtz E L. A comparison of the uterine proteome of mares in oestrus and dioestrus. Reproduction in Domestic Animals = Zuchthygiene 54(3), 473–479.
- Moore S G, Ericsson A C, Poock S E, Melendez P, Lucy M C. Hot topic: 16S rRNA gene sequencing reveals the microbiome of the virgin and pregnant bovine uterus. Journal of Dairy Science 100(6), 4953–4960.
- Morrell J M, Rocha A. A novel approach to minimising acute equine endometritis that may help to prevent the development of the chronic state. Frontiers in Veterinary Science 8, 799619.
- Morris L H A, McCue P M, Aurich C. Equine endometritis: A review of challenges and new approaches. Reproduction (Cambridge, England) 160(5), R95–R110.
- Pascottini O B, Van Schyndel S J, Spricigo J F W, Rousseau J, Weese J S, LeBlanc S J. Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis. Scientific Reports 10(1), 12353.
- Ray K J, Cotter S Y, Arzika A M, Kim J, Bo뫊r N, Zhou Z, Zhong L, Porco T C, Keenan J D, Lietman T M, Doan T. High‐throughput sequencing of pooled samples to determine community‐level microbiome diversity. Annals of Epidemiology 39, 63–68.
- Riddle W T, LeBlanc M M, Stromberg A J. Relationships between uterine culture, cytology and pregnancy rates in a thoroughbred practice. Theriogenology 68(3), 395–402.
- Santos T M, Gilbert R O, Bicalho R C. Metagenomic analysis of the uterine bacterial microbiota in healthy and metritic postpartum dairy cows. Journal of Dairy Science 94(1), 291–302.
- Song Z, Liu Q, Guo H, Ju R, Zhao Y, Li J, Liu X. Tostadin, a novel antibacterial peptide from an antagonistic microorganism Brevibacillus brevis XDH. Bioresource Technology 111, 504–506.
- Traub‐Dargatz J L, Salman M D, Voss J L. Medical problems of adult horses, as ranked by equine practitioners. Journal of the American Veterinary Medical Association 198(10), 1745–1747.
- Weber K S, Wagener K, Blanco M, Bauersachs S, Bollwein H. A comparative analysis of the intrauterine transcriptome in fertile and subfertile mares using cytobrush sampling. BMC Genomics [Electronic Resource] 22(1), 377.
- Wu X C, Qian C D, Fang H H, Wen Y P, Zhou J Y, Zhan Z J, Ding R, Li O, Gao H. Paenimacrolidin, a novel macrolide antibiotic from Paenibacillus sp. F6‐B70 active against methicillin‐resistant Staphylococcus aureus. Microbial Biotechnology 4(4), 491–502.
- Yang X, Yousef A E. Antimicrobial peptides produced by Brevibacillus spp.: Structure, classification and bioactivity: A mini review. World Journal of Microbiology and Biotechnology 34(4), 57.
Citations
This article has been cited 8 times.- Beckers KF, Liu CC, Gomes VCL, Schulz CJ, Childers GW, Fedorka CE, Sones JL. Effects of Intra-uterine Ceftiofur on the Equine Uterine Microbiome. Vet Sci 2025 Aug 30;12(9).
- Yáñez Ramil U, Jezierska S, Krupa M, Bogado Pascottini O. Fundamentals of microbiome-based therapies for reproductive tract inflammatory diseases in domestic animals. Anim Reprod 2025;22(3):e20250030.
- Dyroff AI, López-Valiñas Á, Magalhaes HB, Podico G, Canisso IF, Almiñana C, Bauersachs S. Comparison of RNA- and DNA-based 16S amplicon sequencing to find the optimal approach for the analysis of the uterine microbiome. Sci Rep 2025 May 16;15(1):17037.
- Herzog F, Crissman KR, Beckers KF, Zhou G, Liu CC, Sones JL. Lactobacillus Genus Complex Probiotic-Induced Changes on the Equine Clitoral Microbiome. Vet Sci 2025 Mar 3;12(3).
- da Silva-Álvarez E, Gómez-Arrones V, Correa-Fiz F, Martín-Cano FE, Gaitskell-Phillips G, Carrasco JJ, Rey J, Aparicio IM, Peña FJ, Alonso JM, Ortega-Ferrusola C. Metagenomic and proteomic analyses reveal similar reproductive microbial profiles and shared functional pathways in uterine immune regulation in mares and jennies. PLoS One 2025;20(4):e0321389.
- Gil-Miranda A, Macnicol J, Orellana-Guerrero D, Samper JC, Gomez DE. Reproductive Tract Microbiota of Mares. Vet Sci 2024 Jul 18;11(7).
- Gil-Miranda A, Caddey B, Orellana-Guerrero D, Smith H, Samper JC, Gomez DE. Vaginal and Uterine Microbiota of Healthy Maiden Mares during Estrus. Vet Sci 2024 Jul 18;11(7).
- Wang R, Wang M, Zeng Q, Wang L, Zhang Q, Pu S, Ma X, Wang J, Pan Y. Correlation between microbial characteristics and reproductive status of the yak uterus based on macrogenomic analysis. BMC Vet Res 2024 Jan 3;20(1):4.
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