Effect of different seasons (spring vs summer) on the microbiota diversity in the feces of dairy cows

  • Han Li
  • Rong Li
  • Huijun Chen
  • Jing Gao
  • Yu Wang
  • Yifeng Zhang
  • Zhili QiEmail author
Original Paper


We aimed to study how seasonal heat stress (i.e., spring vs. summer) influenced microbiota diversity in the dairy cows’ feces using Illumina MiSeq sequencing. Sixteen dairy cows were experiencing spring thermoneutral conditions (daily mean temperature = 18.8 ± 3.40 °; daily mean THI = 64.29 ± 4.94) and 16 under summer heat stress (daily mean temperature = 27.63 ± 5.34 °; daily mean THI = 82.56 ± 1.74). Fecal samples were collected per cow three times daily from day 18 to day 22 during each experimental period. Results revealed that the microbiota diversity in the feces was significantly lower (P < 0.05) under summer heat stress. At both the phylum and genera levels, significant differences were observed on microbiota composition in cow’s feces between spring and summer. The most dominant phylum was Firmicutes, contributing 69.45% and 87.14% of the fecal microbiota in spring and summer, respectively, followed by Bacteroidetes, contributing 25.27% and 4.45%, respectively. Compared with the dairy cows in the spring season, the relative abundance of unclassified Peptostreptococcaceae, Turicibacter, and Clostridium_sensu_stricto_1 (P < 0.05) were greatly increased (P < 0.05), while the significant decrease in the proportion of Ruminococcaceae_UCG-005 and Rikenellaceae_RC9_gut_group as well as Bacteroides were observed in hot summer. Prediction of microbiota gene function in feces based on PICRUSt method found that different microbiota between spring and summer were mainly concentrated on the function related to membrane transport, infectious diseases, immune system diseases, and lipid metabolism. This study demonstrates that diversity and composition of fecal microbiota in dairy cows varies under different THI condition, and the relationship between fecal microbiota and cows’ health needs further research.


Dairy cows Fecal microbiota Temperature Humidity Index Illumina MiSeq 


Funding information

This work was supported by the Chinese Key Research and Development Program (2016YFD0500507 and 2018YFD0501605), Fundamental Research Funds for the Central Universities (2662018Y079), and Open Project of Wuhan Academy of Agricultural Sciences (Kfxkt201805).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

The protocol for this experiment was approved by the Institution Animal Care and Use Committee at Huazhong Agriculture University (Wuhan, China), and the animal trial was conducted in accordance with the National Institute of Health Guidelines for the Care and Use of Experiment Animals (Beijing, China).

Supplementary material

484_2019_1812_MOESM1_ESM.pdf (365 kb)
ESM 1 (PDF 365 kb)


  1. Ahmad G, Agarwal A, Esteves S, Sharma R, Almasry M, Al-Gonaim A, AlHayaza G, Singh N, Al Kattan L, Sannaa W, Sabanegh E (2017) Ascorbic acid reduces redox potential in human spermatozoa subjected to heat-induced oxidative stress. Andrologia 49(10):e12773. CrossRefGoogle Scholar
  2. Arumugam M, Raes J, Pelletier E, Paslier DL, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM (2011) Enterotypes of the human gut microbiome. Nature 473:174–180. CrossRefGoogle Scholar
  3. Bishop-Williams KE, Berke O, Pearl DL, Hand K, Kelton DF (2015) Heat stress related dairy cow mortality during heat waves and control periods in rural Southern Ontario from 2010–2012. BMC Vet Res 11(1):291. CrossRefGoogle Scholar
  4. Buffington D, Collazo-Arocho A, Canton G, Pitt D, Thatcher W, Collier R (1981) Black globe-humidity index (BGHI) as comfort equation for dairy cows. Trans ASAE 24(3):711–714CrossRefGoogle Scholar
  5. Calamari L, Morera P, Bani P, Minuti A, Basiricò L, Vitali A, Bernabucci U (2018) Effect of hot season on blood parameters, fecal fermentative parameters, and occurrence of Clostridium tyrobutyricum spores in feces of lactating dairy cows. J Dairy Sci 101(5):4437–4447. CrossRefGoogle Scholar
  6. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621–1624. CrossRefGoogle Scholar
  7. Erickson AR, Cantarel BL, Lamendella R, Darzi Y, Mongodin EF, Pan C, Shah M, Halfvarson J, Tysk C, Henrissat B (2012) Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn’s disease. PLoS One 7(11):e49138. CrossRefGoogle Scholar
  8. Fecteau M-E, Pitta DW, Vecchiarelli B, Indugu N, Kumar S, Gallagher SC, Fyock TL, Sweeney RW (2016) Dysbiosis of the fecal microbiota in cattle infected with Mycobacterium avium subsp. paratuberculosis. PLoS One 11:e0160353. CrossRefGoogle Scholar
  9. Garcia JP, Adams V, Beingesser J, Hughes ML, Poon R, Lyras D, Hill A, Mcclane BA, Rood JI, Uzal FA (2013) Epsilon toxin is essential for the virulence of Clostridium perfringens type D infection in sheep, goats, and mice. Infect Immun 81(7):2405–2414. CrossRefGoogle Scholar
  10. Gonzalez-Rivas PA, Sullivan M, Cottrell JJ, Leury BJ, Gaughan JB, Dunshea FR (2018) Effect of feeding slowly fermentable grains on productive variables and amelioration of heat stress in lactating dairy cows in a sub-tropical summer. Trop Anim Health Prod 50(8):1763–1769. CrossRefGoogle Scholar
  11. Habashy WS, Milfort MC, Adomako K, Attia YA, Rekaya R, Aggrey SE (2017) Effect of heat stress on amino acid digestibility and transporters in meat-type chickens. Poult Sci 96(7):2312–2319. CrossRefGoogle Scholar
  12. Hagey JV, Bhatnagar S, Heguy JM, Karle BM, Price PL, Meyer D, Maga EA (2019) Fecal microbial communities in a large representative cohort of California dairy cows. Front Microbiol 10:1093. CrossRefGoogle Scholar
  13. Henderson G, Cox F, Ganesh S, Jonker A, Young W, Collaborators GRC, Abecia L, Angarita E, Aravena P, Arenas GN (2015) Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci Rep 5(1):14567. CrossRefGoogle Scholar
  14. Jiao J, Li X, Beauchemin KA, Tan Z, Tang S, Zhou C (2015) Rumen development process in goats as affected by supplemental feeding v. grazing: age-related anatomic development, functional achievement and microbial colonisation. Br J Nutr 113(6):888–900. CrossRefGoogle Scholar
  15. Jin W, Wang Y, Li Y, Cheng Y, Zhu W (2018) Temporal changes of the bacterial community colonizing wheat straw in the cow rumen. Anaerobe 50:1–8. CrossRefGoogle Scholar
  16. Kellermayer R, Dowd SE, Harris RA, Balasa A, Schaible TD, Wolcott RD, Tatevian N, Szigeti R, Li Z, Versalovic J (2011) Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice. FASEB J 25(5):1449–1460. CrossRefGoogle Scholar
  17. Khafipour E, Li S, Plaizier JC, Krause DO (2009) Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. J Appl Environ Microbiol 75(22):7115–7124. CrossRefGoogle Scholar
  18. Kim M, Morrison M, Yu Z (2011) Phylogenetic diversity of bacterial communities in bovine rumen as affected by diets and microenvironments. Folia Microbiol 56(5):453. CrossRefGoogle Scholar
  19. Kim M, Morrison M, Yu Z (2015) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol Ecol 76(1):49–63. CrossRefGoogle Scholar
  20. Lee JE, Lee S, Sung J, Ko G (2011) Analysis of human and animal fecal microbiota for microbial source tracking. ISME J 5(2):362. CrossRefGoogle Scholar
  21. Ley RE, Turnbaugh PJ, Samuel K, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023. CrossRefGoogle Scholar
  22. Liu Z, DeSantis TZ, Andersen GL, Knight R (2008) Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers. Nucleic Acids Res 36(18):e120. CrossRefGoogle Scholar
  23. Lu K, Abo RP, Schlieper KA, Graffam ME, Levine S, Wishnok JS, Swenberg JA, Tannenbaum SR, Fox JG (2014) Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ Health Perspect 122(3):284–291. CrossRefGoogle Scholar
  24. Mao S, Zhang R, Wang D, Zhu W (2012) The diversity of the fecal bacterial community and its relationship with the concentration of volatile fatty acids in the feces during subacute rumen acidosis in dairy cows. BMC Vet Res 8(1):237. CrossRefGoogle Scholar
  25. Mao S, Zhang M, Liu J, Zhu W (2015) Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Sci Rep 5:16116. CrossRefGoogle Scholar
  26. Meale SJ, Li S, Azevedo P, Derakhshani H, Plaizier JC, Khafipour E, Steele MA (2016) Development of ruminal and fecal microbiomes are affected by weaning but not weaning strategy in dairy calves. Front Microbiol 7:e84033. CrossRefGoogle Scholar
  27. Milani C, Ticinesi A, Gerritsen J, Nouvenne A, Lugli GA, Mancabelli L, Turroni F, Duranti S, Mangifesta M, Viappiani A (2016) Gut microbiota composition and Clostridium difficile infection in hospitalized elderly individuals: a metagenomic study. Sci Rep 6:25945. CrossRefGoogle Scholar
  28. Pandey P, Hooda O, Kumar S (2017) Impact of heat stress and hypercapnia on physiological, hematological, and behavioral profile of Tharparkar and Karan Fries heifers. Vet World 10(9):1146–1155. CrossRefGoogle Scholar
  29. Patra AK, Yu Z (2015) Essential oils affect populations of some rumen bacteria in vitro as revealed by microarray (RumenBactArray) analysis. Front Microbiol 6:297. CrossRefGoogle Scholar
  30. Plaizier JC, Li S, Danscher AM, Derakshani H, Andersen PH, Khafipour E (2017) Changes in microbiota in rumen digesta and feces due to a grain-based subacute ruminal acidosis (SARA) challenge. Microb Ecol 74(2):485–495. CrossRefGoogle Scholar
  31. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thalliger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. CrossRefGoogle Scholar
  32. Tajima K, Nonaka I, Higuchi K, Takusari N, Kurihara M, Takenaka A, Mitsumori M, Kajikawa H, Aminov RI (2007) Influence of high temperature and humidity on rumen bacterial diversity in Holstein heifers. Anaerobe 13(2):57–64. CrossRefGoogle Scholar
  33. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031. CrossRefGoogle Scholar
  34. Uyeno Y, Sekiguchi Y, Tajima K, Takenaka A, Kurihara M, Kamagata Y (2010) An rRNA-based analysis for evaluating the effect of heat stress on the rumen microbial composition of Holstein heifers. Anaerobe 16(1):27–33. CrossRefGoogle Scholar
  35. Vitali A, Segnalini M, Bertocchi L, Bernabucci U, Nardone A, Lacetera N (2009) Seasonal pattern of mortality and relationships between mortality and temperature-humidity index in dairy cows. J Dairy Sci 92(8):3781–3790. CrossRefGoogle Scholar
  36. Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, Jia W, Cai S, Zhao L (2012) Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 6(2):320–329. CrossRefGoogle Scholar
  37. Wang Y, Xu L, Liu J, Zhu W, Mao S (2017) A high grain diet dynamically shifted the composition of mucosa-associated microbiota and induced mucosal injuries in the colon of sheep. Front Microbiol 8:2080. CrossRefGoogle Scholar
  38. Wu H, Nguyen QD, Tran TT, Tang MT, Tsuruta T, Nishino N (2019) Rumen fluid, feces, milk, water, feed, airborne dust, and bedding microbiota in dairy farms managed by automatic milking systems. Anim Sci J 90:445–452. CrossRefGoogle Scholar
  39. Yazdi MH, Mirzaei-Alamouti H, Amanlou H, Mahjoubi E, Nabipour A, Aghaziarati N, Baumgard L (2016) Effects of heat stress on metabolism, digestibility, and rumen epithelial characteristics in growing Holstein calves. J Anim Sci 94(1):77–89. CrossRefGoogle Scholar
  40. Zhang Y, Wu R, Zhang Y, Wang G, Li K (2018) Impact of nutrient addition on diversity and fate of fecal bacteria. Sci Total Environ 636:717–726. CrossRefGoogle Scholar
  41. Zhu Z, Kristensen L, Difford GF, Poulsen M, Noel SJ, Al-Soud WA, Sørensen SJ, Lassen J, Løvendahl P, Højberg O (2018) Changes in rumen bacterial and archaeal communities over the transition period in primiparous Holstein dairy cows. J Dairy Sci 101(11):9847–9862. CrossRefGoogle Scholar

Copyright information

© ISB 2019

Authors and Affiliations

  1. 1.Department of Animal Nutrition and Feed Science, College of Animal Science and TechnologyHuazhong Agricultural UniversityWuhanChina
  2. 2.Institute of Finance and EconomicsWuhan City Vocational CollegeWuhanChina

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