Abstract
The rumen microbiome is thought to play an important role in maintaining normal gastrointestinal metabolism and nutrient absorption in ruminants. The present study was designed to investigate the effect of heat stress on the rumen microbiome of goats using 16S rRNA sequencing technology. Six female goats were randomly allocated into two control metabolic chambers: A and B (in which the temperature and humidity could be precisely controlled with a precision deviation of ± 0.5 °C and ± 5%, with three goats/chamber). Dynamic changes in the rumen bacterial community were detected under 16 gradually increasing temperature and humidity indexes (THIs). Heat stress had no significant effect on alpha diversity but affected the main phyla and genera of the goat rumen microbiota. With a deeper level of heat stress, the TH groups formed a distinct cluster that differed from that of the control check (CK) group. The dominant phylum transitioned from Firmicutes to Bacteroidetes, and co-exclusion occurred between these two phyla. With the increase in THI, the content of probiotics in the Lachnospiraceae_ND3007_group (P < 0.05) decreased, and the abundance of pathogenic bacteria, such as Erysipelotrichaceae_UCG-004 and Treponema_2, increased; however, the difference between the groups was not significant (P > 0.05). Phylogenetic investigation of communities by reconstruction of unobserved states (PICRUSt) was used to predict bacterial function, and we found that the ambient environment significantly affected the balance between carbohydrate and energy metabolism (P < 0.05). In conclusion, heat stress changed the composition of rumen microbes and affected metabolic function. This experiment provides a theoretical basis for exploring the effects of environmental factors on the rumen of goats.
Similar content being viewed by others
References
Anastassiades T, Rees-Milton K, Hopman WM (2017) The modified amino sugar N-butyryl glucosamine fed to ovariectomized rats preserves bone mineral through increased early mineralization, but does not affect body composition. Funct Foods Health Dis 7:795–815. https://doi.org/10.31989/ffhd.v7i10.377
Avila-Jaime B, Kawas JR, Garcia-Mazcorro JF (2018) Prediction of functional metagenomic composition using archived 16S rDNA sequence data from the gut microbiota of livestock. Livest Sci 213:28–34. https://doi.org/10.1016/j.livsci.2018.04.017
Ballou AL, Ali RA, Mendoza MA, Ellis JC, Hassan HM, Croom WJ, Koci MD (2016) Development of the chick microbiome: how early exposure influences future microbial diversity. Front Vet Sci 3:2. https://doi.org/10.3389/fvets.2016.00002
Belhadj SI, Najar T, Ghram A, Abdrrabba M (2016) Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. J Anim Physiol Anim Nutr 100(3):401–412. https://doi.org/10.1111/jpn.12379
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinform 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Suppl 1):4516–4522. https://doi.org/10.1073/pnas.1000080107
Chan HP, Dong SH, Oh YH, Lee AR, Lee YR, Eun CS (2016) Role of fusobacteria in the serrated pathway of colorectal carcinogenesis. Sci Rep 6:25271. https://doi.org/10.1038/srep25271
Chanda T, Debnath GK, Khan KI, Rahman MM, Chanda GC (2018) Impact of heat stress on milk yield and composition in early lactation of Holstein Friesian crossbred cattle. Bang J Anim Sci 46(3):192–197. https://doi.org/10.3329/bjas.v46i3.36314
Chen Y, Yang F, Lu H, Wang B, Chen Y, Lei D, Wang Y, Zhu B, Li L (2011) Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54(2):562–572. https://doi.org/10.1002/hep.24423
Das R, Sailo L, Verma N, Bharti P, Saikia J, Imtiwati KR (2016) Impact of heat stress on health and performance of dairy animals: a review. Vet World 9(3):260–268. https://doi.org/10.14202/vetworld.2016.260-268
Do HT, Dao KT, Nguyen VKH, Le NG, Nguyen TMP, Le TL, Phung TN, van Straalen NM, Roelofs D, Truong NH (2017) Metagenomic analysis of bacterial community structure and diversity of lignocellulolytic bacteria in Vietnamese native goat rumen. Asian-Aust. J Anim Sci 31(5):738–747. https://doi.org/10.5713/ajas.17.0174
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinform 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Fabris TF, Laporta J, Corra FN, Torres YM, Kirk DJ, McLean DJ, Chapman JD, Dahl GE (2017) Effect of nutritional immunomodulation and heat stress during the dry period on subsequent performance of cows. J Dairy Sci 100(8):6733–6742. https://doi.org/10.3168/jds.2016-12313
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8(7):e1002606. https://doi.org/10.1371/journal.pcbi.1002606
Freestone P, Lyte M (2010) Stress and microbial endocrinology: prospects for ruminant nutrition. Anim 4(7):1248–1257. https://doi.org/10.1017/S1751731110000674
Gabler NK, Koltes D, Schaumberger S, Murugesan GR, Reisinger N (2018) Diurnal heat stress reduces pig intestinal integrity and increases endotoxin translocation. Transl Anim Sci 2:1–10. https://doi.org/10.1093/tas/txx003
Han H, Xiao H, Zhang K, Lu Z (2016) Impact of 4-epi-oxytetracycline on the gut microbiota and blood metabolomics of Wistar rats. Sci Rep 6:23141. https://doi.org/10.1038/srep23141
Iqbal MW, Zhang Q, Yang Y, Li L, Zou C, Huang C, Lin B (2017) Comparative study of rumen fermentation and microbial community differences between water buffalo and Jersey cows under similar feeding conditions. J Appl Anim Res 46(1):740–748. https://doi.org/10.1080/09712119.2017.1394859
Jami E, Mizrahi I (2012) Composition and similarity of bovine rumen microbiota across individual animals. PLoS One 7(3):e33306. https://doi.org/10.1371/journal.pone.0033306
Jami E, Israel A, Kotser A, Mizrahi I (2013) Exploring the bovine rumen bacterial community from birth to adulthood. ISME J 7(6):1069–1079. https://doi.org/10.1038/ismej.2013.2
King CC, Dschaak CM, Eun JS, Fellner PV, Young AJ (2011) Quantitative analysis of microbial fermentation under normal or high ruminal temperature in continuous cultures. Prof Anim Sci 27(4):319–327. https://doi.org/10.15232/S1080-7446(15)30495-2
Kljak K, Pino F, Heinrichs AJ (2017) Effect of forage to concentrate ratio with sorghum silage as a source of forage on rumen fermentation, N balance, and purine derivative excretion in limit-fed dairy heifers. J Dairy Sci 100(1):213–223. https://doi.org/10.3168/jds.2016-11383
Kocherginskaya SA, Aminov RI, White BA (2001) Analysis of the rumen bacterial diversity under two different diet conditions using denaturing gradient gel electrophoresis, random sequencing, and statistical ecology approaches. Anaerobe 7(3):119–134. https://doi.org/10.1006/anae.2001.0378
Koppel N, Rekdal VM, Balskus EP (2017) Chemical transformation of xenobiotics by the human gut microbiota. Science 356(6344):1246–1257. https://doi.org/10.1126/science.aag2770
Lacetera N, Segnalini M, Bernabucci U, Ronchi B, Vitali A, Tran A, Guis H, Caminade C, Calvete C, Morse A, Baylis M, Nardone A (2013) Climate induced effects on livestock population and productivity in the Mediterranean area. In: Navarra A, Tubiana L (eds) Regional assessment of climate change in the Mediterranean. Springer, Dordrecht, pp 135–156
Li F, Li Z, Li S, Ferguson JD, Cao Y, Yao J, Sun F, Wang X, Yang T (2014) Effect of dietary physically effective fiber on ruminal fermentation and the fatty acid profile of milk in dairy goats. J Dairy Sci 97(4):2281–2290. https://doi.org/10.3168/jds.2013-6895
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinform 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Malan SW (2000) The improved Boer goat. Small Rumi Res 36(2):165–170. https://doi.org/10.1016/S0921-4488(99)00160-1
Nonaka I, Takusari N, Tajima K, Suzuki T, Higuchi K, Kurihara M (2008) Effects of high environmental temperatures on physiological and nutritional status of prepubertal Holstein heifers. Livest Sci 113(1):14–23. https://doi.org/10.1016/j.livsci.2007.02.010
O’Brien MD, Rhoads RP, Sanders SR, Duff GC, Baumgard LH (2010) Metabolic adaptations to heat stress in growing cattle. Domest Anim Endocrinol 38(2):86–94. https://doi.org/10.1016/j.domaniend.2009.08.005
Ovreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63(9):3367–3373
Owens FN, Basalan M (2016) Ruminal fermentation. In: Millen DD, Arrigoni MDB, Pacheco RDL (eds) Rumenology. Springer International Publishing, Cham, pp 63–102
Ramayocaldas Y, Mach N, Lepage P, Levenez F, Denis C, Lemonnier G, Leplat JJ, Billon Y, Berri M, Doré J, Rogel-Gaillard C, Estellé J (2016) Phylogenetic network analysis applied to pig gut microbiota identifies an ecosystem structure linked with growth traits. ISME J 10(12):2973–2977. https://doi.org/10.1038/ismej.2016.77
Rubino F, Carberry C, Waters SM, Kenny D, McCabe MS, Creevey CJ (2017) Divergent functional isoforms drive niche specialisation for nutrient acquisition and use in rumen microbiome. ISME J 11(4):932–944. https://doi.org/10.1038/ismej.2016.172
Seibert JT, Abuajamieh M, Sanz Fernandez MV, Johnson JS, Kvidera SK, Horst EA, Mayorga EJ, Lei S, Patience JF, Ross JW, Rhoads RP, Johnson RC, Lonergan SM, Perfield JW 2nd, Baumgard LH (2018) Effects of heat stress and insulin sensitizers on pig adipose tissue. J Anim Sci 96(2):510–520. https://doi.org/10.1093/jas/skx067
Soren NM, Sejian V, Terhuja M, Dominic G (2017) Enteric methane emission in sheep: process description and factors influencing production. In: Sejian V, Bhatta R, Gaughan J, Malik P, Naqvi S, Lal R (eds) Sheep production adapting to climate change. Springer, Singapore, pp 209–233
Su J, Wei Y, Liu M, Liu T, Li J, Ji Y, Liang J (2014) Anti-hyperuricemic and nephroprotective effects of Rhizoma Dioscoreae septemlobae, extracts and its main component dioscin via regulation of mOAT1, mURAT1 and mOCT2 in hypertensive mice. Arch Pharm Res 37(10):1336–1344. https://doi.org/10.1007/s12272-014-0413-6
Sun Y, Xie B, Wang M, Dong C, Du X, Fu Y, Liu H (2016) Microbial community structure and succession of airborne microbes in closed artificial ecosystem. Ecol Eng 88:165–176. https://doi.org/10.1016/j.ecoleng.2015.12.013
Tajima K, Aminov RI, Nagamine T, Matsui H, Nakamura M, Benno Y (2001) Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Appl Environ Microbiol 67(6):2766–2774. https://doi.org/10.1128/AEM.67.6.2766-2774.2001
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. https://doi.org/10.1016/j.anaerobe.2006.12.001
Tucker CB, Rogers AR, Schütz KE (2008) Effect of solar radiation on dairy cattle behaviour, use of shade and body temperature in a pasture-based system. Appl Anim Behav Sci 109(2–4):141–154. https://doi.org/10.1016/j.applanim.2007.03.015
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. https://doi.org/10.1016/j.anaerobe.2009.04.006
Verhalen B, Dastvan R, Thangapandian S, Peskova Y, Koteiche HA, Nakamoto RK, Tajkhorshid E, Mchaourab HS (2017) Energy transduction and alternating access of the mammalian ABC transporter p-glycoprotein. Nature 543(7647):738–741. https://doi.org/10.1038/nature21414
Wang L, Qin X, Kong F, Yang Y, Wu D, Mishra S, Li Y (2016) Exploring the goat rumen microbiome from seven days to two years. PLoS One 11(5):e0154354. https://doi.org/10.1371/journal.pone.0154354
Wang Y, Cao P, Wang L, Zhao Z, Chen Y, Yang Y (2017) Bacterial community diversity associated with different levels of dietary nutrition in the rumen of sheep. Appl Microbiol Biotechnol 101(9):3717–3728. https://doi.org/10.1007/s00253-017-8144-5
Wang XJ, Feng JH, Zhang MH, Li XM, Ma DD, Chang SS (2018) Effects of high ambient temperature on the community structure and composition of ileal microbiome of broilers. Poult Sci 97(6):2153–2158. https://doi.org/10.3382/ps/pey032
Wenz T (2013) Regulation of mitochondrial biogenesis and PGC-1α under cellular stress. Mitochondrion 13(2):134–142. https://doi.org/10.1016/j.mito.2013.01.006
Zhang X, Sukhchuluun G, Bo T, Chi Q, Yang J, Chen B, Zhang L, Wang D (2018) Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome 6(1):103. https://doi.org/10.1186/s40168-018-0473-9
Acknowledgments
We thank Jinpeng Li and Guojun Wang for their powerful help during sample collection and Yunjia Li for graphics support.
Funding
This study was financially supported by the National Key Research and Development Program of China (2016YFD0500508) and China Agriculture Research System (CARS-39-12).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All Experimental Animal Management Committee of Northwest A&F University guidelines for the care and experimental procedures of animals were followed.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 1.51 mb)
Rights and permissions
About this article
Cite this article
Zhong, S., Ding, Y., Wang, Y. et al. Temperature and humidity index (THI)-induced rumen bacterial community changes in goats. Appl Microbiol Biotechnol 103, 3193–3203 (2019). https://doi.org/10.1007/s00253-019-09673-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-09673-7