A common vaginal microbiota composition among breeds of Bos taurus indicus (Gyr and Nellore)
Describing the bovine vaginal microbiota is essential to better understand its physiology and its impact on health maintenance. Despite the economic importance of reproduction of these animals, bovine vaginal microbial community is still poorly described in comparison with rumen microbiome. Previous studies of our group described the vaginal microbiota of Nellore, an important Bos taurus indicus breed, using metagenomics. In order to better understand this microbiota, the present work aims to investigate another important breed, Gyr. Results have shown bacterial dominance over Archaea and Fungi was observed, with the most abundant bacterial phylum (Firmicutes) representing 40–50% of bacterial population, followed by Bacteroidetes, Proteobacteria, and Actinobacteria. The Fungi kingdom had the Mycosphaerella genus as its main representative, followed by Cladosporium. Archaea were observed at a very low abundance in all animals, with a high relative abundance of Methanobrevibacter genus. These results demonstrate a high microbial diversity on vaginal tract of Gyr, as demonstrated for Nellore and different from the previously described for other species. Our results indicate a great similarity between vaginal microbiota of Nellore and Gyr despite the differences in animal handling and genetic improvement. As observed for both breeds, individual variation is the largest source of microbial diversity between animals.
KeywordsMicrobiota Metagenomics Bovine Gyr Vaginal tract
The study was supported by grants from the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
Conceived and designed the experiments: SGF, MLN, JRN, GCO and EFBS. Performed the experiments: SGF, MLN, MRG, FMGA, ACMS and APO. Analyzed the data: SGF, MLN and LRL. Contributed reagents/materials/analysis tools: JRN, GCO, FGF and EFBS. Wrote the paper: SGF, MLN, JRN, GCO, FGF and EFBS. All authors reviewed the manuscript.
This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant ID 473879/2013-1).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving animals were in accordance with the ethical standards of Ethics Committee in Animal Experimentation of the Universidade Federal de Minas Gerais, Brazil (CETEA/UFMG - 95/2012) at which the studies were conducted.
- 2.Loaces I, Amarelle V, Muñoz-Gutierrez I, Fabiano E, Martinez A, Noya F (2015) Improved ethanol production from biomass by a rumen metagenomic DNA fragment expressed in Escherichia coli MS04 during fermentation. Appl Microbiol Biotechnol 99:9049–9060. https://doi.org/10.1007/s00253-015-6801-0 CrossRefPubMedGoogle Scholar
- 3.Roehe R, Dewhurst RJ, Duthie CA, Rooke JA, McKain N, Ross DW, Hyslop JJ, Waterhouse A, Freeman TC, Watson M, Wallace RJ (2016) Bovine host genetic variation influences rumen microbial methane production with best selection criterion for low methane emitting and efficiently feed converting hosts based on metagenomic gene abundance. PLoS Genet 12:e1005846. https://doi.org/10.1371/journal.pgen.1005846 CrossRefPubMedPubMedCentralGoogle Scholar
- 5.Laguardia-Nascimento M, Branco KMGR, Gasparini MR, Giannattasio-Ferraz S, Leite LR, Araujo FMG, Salim ACM, Nicoli JR, de Oliveira GC, Barbosa-Stancioli EF (2015) Vaginal microbiome characterization of Nellore cattle using metagenomic analysis. PLoS One 10:e0143294. https://doi.org/10.1371/journal.pone.0143294 CrossRefPubMedPubMedCentralGoogle Scholar
- 6.Bicalho ML, Santin T, Rodrigues MX, Marques CE, Lima SF, Bicalho RC (2017) Dynamics of the microbiota found in the vaginas of dairy cows during the transition period: associations with uterine diseases and reproductive outcome. J Dairy Sci 100:3043–3058. https://doi.org/10.3168/jds.2016-11623 CrossRefPubMedGoogle Scholar
- 10.Dumonceaux TJ, Schellenberg J, Goleski V, Hill JE, Jaoko W, Kimani J, Money D, Ball TB, Plummer FA, Severini A (2009) Multiplex detection of bacteria associated with normal microbiota and with bacterial vaginosis in vaginal swabs by use of oligonucleotide-coupled fluorescent microspheres. J Clin Microbiol 47:4067–4077. https://doi.org/10.1128/JCM.00112-09 CrossRefPubMedPubMedCentralGoogle Scholar
- 11.Branco KMGR, Nardi RMD, Moreira JLS, Nunes AC, Farias LM, Nicoli JR, Carvalho MAR (2010) Identification and in vitro production of Lactobacillus antagonists from women with or without bacterial vaginosis. Braz J Med Biol Res 43:338–344. https://doi.org/10.1590/S0100-879X2010007500013 CrossRefPubMedGoogle Scholar
- 12.Miller EA, Beasley DE, Dunn RR, Archie EA (2016) Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique? Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01936
- 13.Spear GT, Kersh E, Guenthner P, Vishwanathan SA, Gilbert D, Zariffard MR, Mirmonsef P, Landay A, Zheng L, Gillevet P (2012) Longitudinal assessment of pigtailed macaque lower genital tract microbiota by pyrosequencing reveals dissimilarity to the genital microbiota of healthy humans. AIDS Res Hum Retrovir 28:1244–1249. https://doi.org/10.1089/aid.2011.0382 CrossRefPubMedGoogle Scholar
- 14.Yildirim S, Yeoman CJ, Janga SC, Thomas SM, Ho M, Leigh SR, Consortium PM, White BA, Wilson BA, Stumpf RM (2014) Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance. ISME J 8:2431–2444. https://doi.org/10.1038/ismej.2014.90 CrossRefPubMedPubMedCentralGoogle Scholar
- 15.Swartz JD, Lachman M, Westveer K, O’Neill T, Geary T, Kott R et al (2014) Characterization of the vaginal microbiota of ewes and cows reveals a unique microbiota with low levels of lactobacilli and near-neutral pH. Front Vet Sci 1. https://doi.org/10.3389/fvets.2014.00019
- 18.Amin JD, Zaria LT, Malgwi RM (1996) Vaginal aerobic bacterial flora of apparently healthy cattle in various stages of the reproductive cycle in the Sahel region of Nigeria. Bull Anim Heal Prod Africa 44:15–18Google Scholar
- 21.Sharda R, Monghe MN, Tanwani SK (1991) Antibiotic sensitivity pattern of bacteria isolated from repeat breeding animals. Indian Vet J 68:197–200Google Scholar
- 23.Faveri M, Gonçalves LFH, Feres M, Figueiredo LC, Gouveia LA, Shibli JA, Mayer MP (2011) Prevalence and microbiological diversity of archaea in peri-implantitis subjects by 16S ribosomal RNA clonal analysis. J Periodontal Res 46:338–344. https://doi.org/10.1111/j.1600-0765.2011.01347.x CrossRefPubMedGoogle Scholar
- 24.Kwiatkowski NP, Babiker WM, Merz WG, Carroll KC, Zhang SX (2012) Evaluation of nucleic acid sequencing of the D1/D2 region of the large subunit of the 28S rDNA and the internal transcribed spacer region using smartgene idn software for identification of filamentous fungi in a clinical laboratory. J Mol Diagnostics 14:393–401. https://doi.org/10.1016/j.jmoldx.2012.02.004 CrossRefGoogle Scholar
- 25.Meyer F, Paarmann D, D’Souza M, Oslon R, Kubal M et al (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinf 9. https://doi.org/10.1186/1471-2105-9-386
- 28.Verkley JMG, Crous PW, Groenewald JZ, Braun U, Aptroot A (2004) Mycosphaerella punctiformis revisited: morphology, phylogeny, and epitypification of the type species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycol Res 108:1271–1282. https://doi.org/10.1017/S0953756204001054 CrossRefPubMedGoogle Scholar
- 29.Dias J, Marcondes MI, Noronha MF, Resende RT, Machado FS, Mantovani HC, Dill-McFarland KA, Suen G (2017) Effect of pre-weaning diet on the ruminal archaeal, bacterial, and fungal communities of dairy calves. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.01553
- 30.Miñana-Galbis D, Pinzón DL, Lorén JG, Manresa A, Oliart-Ros RM (2010) Reclassification of Geobacillus pallidus (Scholz et al. 1988) Banat et al. 2004 as Aeribacillus pallidus gen. Nov., comb. nov. Int J Syst Evol Microbiol 60:1600–1604. https://doi.org/10.1099/ijs.0.003699-0 CrossRefPubMedGoogle Scholar
- 33.Oikonomou G, Bicalho ML, Meira E, Rossi RE, Foditsch C, Machado VS, Teixeira AGV, Santisteban C, Schukken YH, Bicalho RC (2014) Microbiota of Cow’s Milk; distinguishing healthy, sub-clinically and clinically diseased quarters. PLoS One 9. https://doi.org/10.1371/journal.pone.0085904 CrossRefGoogle Scholar
- 35.Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua K, Kachman SD, Moriyama EN, Walter J, Peterson DA, Pomp D (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PNAS. 107:18933–18938. https://doi.org/10.1073/pnas.1007028107 CrossRefPubMedGoogle Scholar
- 37.Pereira CB, Pereira-de-Sá N, Borelli BM, Rosa CA, Barbeira PJ, Cota BB, Johann S (2016) Antifungal activity of eicosanoic acids isolated from the endophytic fungus Mycosphaerella sp. against Cryptococcus neoformans and C. gattii. Microb Pathog 100:205–212. https://doi.org/10.1016/j.micpath.2016.09.022 CrossRefPubMedGoogle Scholar
- 41.Dridi B, Henry M, El Khéchine A, Raoult D, Drancourt M (2009) High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLoS One 4:e7063. https://doi.org/10.1371/journal.pone.0007063 CrossRefPubMedPubMedCentralGoogle Scholar
- 43.Carberry CA, Kenny DA, Kelly AK, Waters SM (2014) Quantitative analysis of ruminal methanogenic microbial populations in beef cattle divergent in phenotypic residual feed intake (RFI) offered contrasting diets. J Anim Sci Biotechnol 5:41. https://doi.org/10.1186/2049-1891-5-41 CrossRefPubMedPubMedCentralGoogle Scholar