Characterization of the seminal bacterial microbiome of healthy, fertile stallions using next-generation sequencing
Carlota Quiñones-Pérez; Manuel Hidalgo; Isabel Ortiz; Francisco Crespo; José Luis Vega-Pla
Abstract
Keywords
References
Al Jassim RAM, Andrews FM. The bacterial community of the horse gastrointestinal tract and its relation to fermentative acidosis, laminitis, colic, and stomach ulcers. Vet Clin North Am Equine Pract. 2009;25(2):199-215.
Al-Kass Z, Eriksson E, Bagge E, Wallgren M, Morrell JM. Bacteria detected in the genital tract, semen or pre-ejaculatory fluid of Swedish stallions from 2007 to 2017. Acta Vet Scand. 2019;61(1):25.
Al-Kass Z, Guo Y, Vinnere Pettersson O, Niazi A, Morrell JM. Metagenomic analysis of bacteria in stallion semen. Anim Reprod Sci. 2020;221:106568.
Althouse C, Skaife J, Loomis P. Prevalence and types of contaminant bacteria in extended, chilled equine semen. Anim Reprod Sci. 2010;121(1, Suppl):224-5.
Bag S, Saha B, Mehta O, Anbumani D, Kumar N, Dayal M, Pant A, Kumar P, Saxena S, Allin KH, Hansen T, Arumugam M, Vestergaard H, Pedersen O, Pereira V, Abraham P, Tripathi R, Wadhwa N, Bhatnagar S, Prakash VG, Radha V, Anjana RM, Mohan V, Takeda K, Kurakawa T, Nair GB, Das B. An improved method for high quality metagenomics DNA extraction from human and environmental samples. Sci Rep. 2016;6:26775.
Barba M, Martínez-Boví R, Quereda JJ, Mocé ML, Plaza-Dávila M, Jiménez-Trigos E, Gómez-Martín Á, González-Torres P, Carbonetto B, García-Roselló E. Vaginal Microbiota Is Stable throughout the Estrous Cycle in Arabian Maress. Animals (Basel). 2020;10(11):2020.
Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci USA. 2014;111(6):2200-5.
Costa MC, Weese JS. The equine intestinal microbiome. Anim Health Res Rev. 2012;13(1):121-8.
Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease. Vet Clin North Am Equine Pract. 2018;34(1):1-12.
Coverdale JA. HORSE SPECIES SYMPOSIUM: can the microbiome of the horse be altered to improve digestion? J Anim Sci. 2016;94(6):2275-81.
Daly K, Stewart CS, Flint HJ, Shirazi-Beechey SP. Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes. FEMS Microbiol Ecol. 2001;38(2):141-51.
Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A microbiological map of the healthy equine gastrointestinal tract. PLoS One. 2016 Nov 15;11(11):e0166523.
Espinosa CI. Medidas de Alpha diversidad [Internet]. Ecología en Práctica; 2019 [cited 2021 Apr 12]. Available from:
Fullston T, McPherson NO, Owens JA, Kang WX, Sandeman LY, Lane M. Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet. Physiol Rep. 2015;3(3):e12336.
Goulet O. Potential role of the intestinal microbiota in programming health and disease. Nutr Rev. 2015;73(Suppl 1):32-40.
Hou D, Zhou X, Zhong X, Settles ML, Herring J, Wang L, Abdo Z, Forney LJ, Xu C. Microbiota of the seminal fluid from healthy and infertile men. Fertil Steril. 2013;100(5):1261-9.
Ivanov IB, Kuzmin MD, Gritsenko VA. Microflora of the seminal fluid of healthy men and men suffering from chronic prostatitis syndrome. Int J Androl. 2009;32(5):462-7.
Jarvi K, Lacroix JM, Jain A, Dumitru I, Heritz D, Mittelman MW. Polymerase chain reaction-based detection of bacteria in semen. Fertil Steril. 1996;66(3):463-7.
Javurek AB, Spollen WG, Ali AMM, Johnson SA, Lubahn DB, Bivens NJ, Bromert KH, Ellersieck MR, Givan SA, Rosenfeld CS. Discovery of a Novel Seminal Fluid Microbiome and Influence of Estrogen Receptor Alpha Genetic Status. Sci Rep. 2016;6(1):23027.
Kiessling AA, Desmarais BM, Yin H-Z, Loverde J, Eyre RC. Detection and identification of bacterial DNA in semen. Fertil Steril. 2008;90(5):1744-56.
LaFrentz S, Abarca E, Mohammed HH, Cuming R, Arias CR. Characterization of the normal equine conjunctival bacterial community using culture-independent methods. Vet Ophthalmol. 2020;23(3):480-8.
Liu CM, Osborne BJW, Hungate BA, Shahabi K, Huibner S, Lester R, Dwan MG, Kovacs C, Contente-Cuomo TL, Benko E, Aziz M, Price LB, Kaul R. The semen microbiome and its relationship with local immunology and viral load in HIV infection. PLoS Pathog. 2014;10(7):e1004262.
Maasen M, Christensen P. Bacterial flora of semen collected from Danish warmblood stallions by artificial vagina. Acta Vet Scand. 1995;36(1):1-7.
Mändar R, Punab M, Borovkova N, Lapp E, Kiiker R, Korrovits P, Metspalu A, Krjutškov K, Nõlvak H, Preem JK, Oopkaup K, Salumets A, Truu J. Complementary seminovaginal microbiome in couples. Res Microbiol. 2015;166(5):440-7.
Mändar R. Microbiota of male genital tract: impact on the health of man and his partner. Pharmacol Res. 2013;69(1):32-41.
Manguin E, Pépin E, Boivin R, Leclere M. Tracheal microbial populations in horses with moderate asthma. J Vet Intern Med. 2020;34(2):986-95.
Milinovich GJ, Klieve AV, Pollitt CC, Trott DJ. Microbial events in the hindgut during carbohydrate-induced equine laminitis. Vet Clin North Am Equine Pract. 2010;26(1):79-94.
Mira Obrador A. Análisis taxonómico y funcional humano mediante aproximaciones clásiclas moleculares y metagenómica. Valencia: Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunidad Valenciana; 2014.
Moretti E, Capitani S, Figura N, Pammolli A, Federico MG, Giannerini V, Collodel G. The presence of bacteria species in semen and sperm quality. J Assist Reprod Genet. 2009;26(1):47-56.
Ng S-F, Lin RCY, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature. 2010;467(7318):963-6.
Ortega-Ferrusola C, González-Fernández L, Muriel A, Macías-García B, Rodríguez-Martínez H, Tapia JA, Alonso JM, Peña FJ. Does the microbial flora in the ejaculate affect the freezeability of stallion sperm? Reprod Domest Anim. 2009;44(3):518-22.
Pasing SS, Aurich C, von Lewinski M, Wulf M, Krüger M, Aurich JE. Development of the genital microflora in stallions used for artificial insemination throughout the breeding season. Anim Reprod Sci. 2013;139(1–4):53-61.
Pickett BW, Voss JL, Jones RL. Control of bacteria in stallions and their semen. J Equine Vet Sci. 1999;19(7):424-69.
Rando OJ, Simmons RA. I’m eating for two: parental dietary effects on offspring metabolism. Cell. 2015;161(1):93-105.
Rando OJ. Daddy issues: paternal effects on phenotype. Cell. 2012;151(4):702-8.
Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci. 2013;33(21):9003-12.
Rosenfeld CS, Javurek AB, Johnson SA, Lei Z, Sumner LW, Hess RA. Seminal fluid metabolome and epididymal changes after antibiotic treatment in mice. Reproduction. 2018;156(1):1-10.
Rota A, Calicchio E, Nardoni S, Fratini F, Ebani VV, Sgorbini M, Panzani D, Camillo F, Mancianti F. Presence and distribution of fungi and bacteria in the reproductive tract of healthy stallions. Theriogenology. 2011;76(3):464-70.
Salem SE, Maddox TW, Antczak P, Ketley JM, Williams NJ, Archer DC. Acute changes in the colonic microbiota are associated with large intestinal forms of surgical colic. BMC Vet Res. 2019;15(1):468.
Samper JC. Equine breeding management and artificial insemination. USA: Elsevier Health Sciences; 2009. 336 p.
Sanocka-Maciejewska D, Ciupińska M, Kurpisz M. Bacterial infection and semen quality. J Reprod Immunol. 2005;67(1–2):51-6.
Serrano M, Climent E, Freire F, Martínez-Blanch JF, González C, Reyes L, Solaz-Fuster MC, Calvo JH, Jiménez MÁ, Codoñer FM. Influence of the ovine genital tract microbiota on the species artificial insemination outcome. A pilot study in commercial sheep farms. High Throughput. 2020;9(3):16.
Sharma S, Dhaliwal GS, Dadarwal D. Reproductive efficiency of Thoroughbred mares under Indian subtropical conditions: a retrospective survey over 7 years. Anim Reprod Sci. 2010;117(3–4):241-8.
Su S, Zhao Y, Liu Z, Liu G, Du M, Wu J, Bai D, Li B, Bou G, Zhang X, Dugarjaviin M. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments of Mongolian horses. MicrobiologyOpen. 2020;9(6):e1020.
Swyers KL, Burk AO, Hartsock TG, Ungerfeld EM, Shelton JL. Effects of direct-fed microbial supplementation on digestibility and fermentation end-products in horses fed low- and high-starch concentrates. J Anim Sci. 2008;86(10):2596-608.
Thermo Fisher Scientific. Ion Reporter Software 5.18.1.0 [software]. 2021 [cited 2021 Jul 20]. Available from:
Tomaiuolo R, Veneruso I, Cariati F, D’Argenio V. Microbiota and human reproduction: the case of male infertility. High Throughput; 2020;9(2):10.
Varela E, Rey J, Plaza E, Muñoz de Propios P, Ortiz-Rodríguez JM, Álvarez M, Anel-López L, Anel L, De Paz P, Gil MC, Morrell JM, Ortega-Ferrusola C. How does the microbial load affect the quality of equine cool-stored semen? Theriogenology. 2018;114:212-20.
Varner DD, Scanlan CM, Thompson JA, Brumbaugh GW, Blanchard TL, Carlton CM, Johnson L. Bacteriology of preserved stallion semen and antibiotics in semen extenders. Theriogenology. 1998;50(4):559-73.
Weng S-L, Chiu C-M, Lin F-M, Huang W-C, Liang C, Yang T, Yang TL, Liu CY, Wu WY, Chang YA, Chang TH, Huang HD. Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PLoS One. 2014 Oct 23;9(10):e110152.
Wickware CL, Johnson TA, Koziol JH. Composition and diversity of the preputial microbiota in healthy bulls. Theriogenology. 2020;145:231-7.
Wu X, Zhang H, Chen J, Shang S, Wei Q, Yan J, Tu X. Comparison of the fecal microbiota of dholes high-throughput Illumina sequencing of the V3-V4 region of the 16S rRNA gene. Appl Microbiol Biotechnol. 2016;100(8):3577-86.
Zhang D, Ji H, Liu H, Wang S, Wang J, Wang Y. Changes in the diversity and composition of gut microbiota of weaned piglets after oral administration of Lactobacillus or an antibiotic. Appl Microbiol Biotechnol. 2016;100(23):10081-93.
Submitted date:
12/10/2020
Accepted date:
06/22/2021