Microbial diversity within the digestive tract contents of Dezhou donkeys


Autoři: Guiqin Liu aff001;  Gerelchimeg Bou aff001;  Shaofeng Su aff001;  Jingya Xing aff002;  Honglei Qu aff003;  Xinzhuang Zhang aff001;  Xisheng Wang aff001;  Yiping Zhao aff001;  Manglai Dugarjaviin aff001
Působiště autorů: College of Animal Science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, China aff001;  College of Agronomy, Liaocheng University, Shandong Engineering Technology Research Center for Efficient Breeding and Ecological Feeding of Black Donkey, Shandong Donkey Industry Technology Collaborative Innovation Center, Liaocheng, Shandong Province, Ch aff002;  National Engineering Research Center for Gelatin-based Traditional Chinese Medicine, Dong-E-E-Jiao Co. Ltd., Dong-E Country, Shandong Province, China aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226186

Souhrn

Gastrointestinal microbiota has significant impact on the nutrition and health of monogastric herbivores animals including donkey. However, so far the microbiota in different gastrointestinal compartments of healthy donkey has not been described. Therefore, we investigated the abundance and function of microbiota at different sites of the gastrointestinal tract (GIT) (foregut: stomach, duodenum, jejunum and ileum; hindgut: cecum, ventral colon, dorsal colon, and rectum) of healthy adult donkeys mainly based on 16S rRNA gene sequencing and phylogenetic investigation of communities by reconstruction of unobserved states (PICRUSt) analysis. Collectively, our results showed that donkey has a rich, diverse and multi-functional microbiota along the GIT. In general, the richness and diversity of the microbiota are much higher in the hindgut relative to that in the foregut; at phylum level, the Firmicutes is dominant in the foregut while both Firmicutes and Bacteroides are abundant in the hindgut; at the genus level, Lactobacillus was dominant in the foregut while Streptococcus was more dominant in the hindgut. Our further PICRUSt analysis showed that varying microbiota along the GIT is functionally compatible with the corresponding physiological function of different GIT sites. For example, the microbes in the foregut are more active at carbohydrate metabolism, and in the hindgut are more active at amino acid metabolism. This work at the first time characterized the donkey digestive system from the aspects of microbial composition and function, provided an important basic data about donkey healthy gastrointestinal microbiota, which may be utilized to evaluate donkey health and also offer clues to further investigate donkey digestive system, nutrition, even to develop the microbial supplements.

Klíčová slova:

Asses – Carbohydrate metabolism – Cecum – Colon – Microbiome – Rectum – Sequence databases – Species diversity


Zdroje

1. Costa MC, Weese JS. Understanding the Intestinal Microbiome in Health and Disease. The Veterinary clinics of North America Equine practice. 2018;34(1):1–12. doi: 10.1016/j.cveq.2017.11.005 29402480.

2. W ZX, C YQ, Q HL, C YG, F YL, L WQ, et al. Research progress of nutrient requirements of donkeys. Journal of Liaocheng University. 2018;31(03):109–13.

3. Argenzio RA, Southworth M, Stevens CE. Sites of organic acid production and absorption in the equine gastrointestinal tract. The American journal of physiology. 1974;226(5):1043–50. doi: 10.1152/ajplegacy.1974.226.5.1043 4824856.

4. Bergman H, Gustavsson I. Variable starch gel electrophoretic pattern of the enzyme 6-phosphogluconate dehydrogenase in a family of donkeys (Equus asinus L.). Hereditas. 1972;67(1):145–6. doi: 10.1111/j.1601-5223.1971.tb02367.x 4680625.

5. Julliand V, de Vaux A, Millet L, Fonty G. Identification of Ruminococcus flavefaciens as the predominant cellulolytic bacterial species of the equine cecum. Applied and environmental microbiology. 1999;65(8):3738–41. 10427077; PubMed Central PMCID: PMC91562.

6. Costa MC, Silva G, Ramos RV, Staempfli HR, Arroyo LG, Kim P, et al. Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses. Veterinary journal. 2015;205(1):74–80. doi: 10.1016/j.tvjl.2015.03.018 25975855.

7. Zhang J, Shi H, Wang Y, Cao Z, Yang H, Li S. Effect of Limit-Fed Diets With Different Forage to Concentrate Ratios on Fecal Bacterial and Archaeal Community Composition in Holstein Heifers. Front Microbiol. 2018;9:976. doi: 10.3389/fmicb.2018.00976 29867879; PubMed Central PMCID: PMC5962747.

8. Liu X, Fan H, Ding X, Hong Z, Nei Y, Liu Z, et al. Analysis of the gut microbiota by high-throughput sequencing of the V5-V6 regions of the 16S rRNA gene in donkey. Current microbiology. 2014;68(5):657–62. doi: 10.1007/s00284-014-0528-5 24452427.

9. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, et al. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141(7):1241–52. doi: 10.1016/j.cell.2010.05.005 20603004; PubMed Central PMCID: PMC2900928.

10. Aydin A, Pekel AY, Issa G, Demirel G, Patterson PH. Effects of dietary copper, citric acid, and microbial phytase on digesta pH and ileal and carcass microbiota of broiler chickens fed a low available phosphorus diet. The Journal of Applied Poultry Research. 2010;19(4):422–31. doi: 10.3382/japr.2009-00123

11. Dawson AM, Trenchard D, Guz A. Small bowel tonometry: assessment of small gut mucosal oxygen tension in dog and man. Nature. 1965;206(987):943–4. doi: 10.1038/206943b0 5839858.

12. Wu S, Baldwin RL, Li WZ, Li CJ, Conner EE, Li RW. The bacterial community composition of the bovine rumen detected using pyrosequencing of 16S rRNA genes. Metagenomics. 2012;1:1–11.

13. Castro-Carrera T, Toral PG, Frutos P, McEwan NR, Hervas G, Abecia L, et al. Rumen bacterial community evaluated by 454 pyrosequencing and terminal restriction fragment length polymorphism analyses in dairy sheep fed marine algae. Journal of dairy science. 2014;97(3):1661–9. doi: 10.3168/jds.2013-7243 24440247.

14. An D, Dong X, Dong Z. Prokaryote diversity in the rumen of yak (Bos grunniens) and Jinnan cattle (Bos taurus) estimated by 16S rDNA homology analyses. Anaerobe. 2005;11(4):207–15. doi: 10.1016/j.anaerobe.2005.02.001 16701570.

15. Li ZP, Liu HL, Li GY, Bao K, Wang KY, Xu C, et al. Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China. BMC microbiology. 2013;13:151. doi: 10.1186/1471-2180-13-151 23834656; PubMed Central PMCID: PMC3723558.

16. Sundset MA, Praesteng KE, Cann IK, Mathiesen SD, Mackie RI. Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microbial ecology. 2007;54(3):424–38. doi: 10.1007/s00248-007-9254-x 17473904.

17. Ericsson AC, Johnson PJ, Lopes MA, Perry SC, Lanter HR. A Microbiological Map of the Healthy Equine Gastrointestinal Tract. PloS one. 2016;11(11):e0166523. doi: 10.1371/journal.pone.0166523 27846295; PubMed Central PMCID: PMC5112786.

18. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal; Vol 17, No 1: Next Generation Sequencing Data AnalysisDO—1014806/ej171200. 2011.

19. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–200. doi: 10.1093/bioinformatics/btr381 21700674; PubMed Central PMCID: PMC3150044.

20. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome research. 2011;21(3):494–504. doi: 10.1101/gr.112730.110 21212162; PubMed Central PMCID: PMC3044863.

21. Edgar R. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature methods. 2013;10(10):996–8. doi: 10.1038/nmeth.2604 23955772.

22. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and environmental microbiology. 2007;73(16):5261–7. doi: 10.1128/AEM.00062-07 17586664; PubMed Central PMCID: PMC1950982.

23. Edgar R. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147; PubMed Central PMCID: PMC390337.

24. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature biotechnology. 2013;31(9):814–21. doi: 10.1038/nbt.2676 23975157; PubMed Central PMCID: PMC3819121.

25. Qi Z, Shi SQ, Tu J, Li SW. Comparative metagenomic sequencing analysis of cecum microbiotal diversity and function in broilers and layers. 3 Biotech. 2019;9(8):316. doi: 10.1007/s13205-019-1834-1 31406638; PubMed Central PMCID: PMC6669222.

26. Costa MC, Arroyo LG, Allen-Vercoe E, Stampfli HR, Kim PT, Sturgeon A, et al. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene. PloS one. 2012;7(7):e41484. doi: 10.1371/journal.pone.0041484 22859989; PubMed Central PMCID: PMC3409227.

27. Shepherd ML, Swecker WS Jr., Jensen RV, Ponder MA. Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons. FEMS microbiology letters. 2012;326(1):62–8. doi: 10.1111/j.1574-6968.2011.02434.x 22092776.

28. Rawls JF, Mahowald MA, Ley RE, Gordon JI. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 2006;127(2):423–33. doi: 10.1016/j.cell.2006.08.043 17055441; PubMed Central PMCID: PMC4839475.

29. Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PloS one. 2008;3(7):e2836. doi: 10.1371/journal.pone.0002836 18665274; PubMed Central PMCID: PMC2475661.

30. IS M. Implications of dietary fiber and fermentable carbohydrates on gut health and intestinal microbial ecology of the dog: University of Illinois at Urbana-Champaign; 2008.

31. Dougal K, Harris PA, Edwards A, Pachebat JA, Blackmore TM, Worgan HJ, et al. A comparison of the microbiome and the metabolome of different regions of the equine hindgut. FEMS microbiology ecology. 2012;82(3):642–52. doi: 10.1111/j.1574-6941.2012.01441.x 22757649.

32. DiBaise JK, Zhang H, Crowell MD, Krajmalnik-Brown R, Decker GA, Rittmann BE. Gut microbiota and its possible relationship with obesity. Mayo Clinic proceedings. 2008;83(4):460–9. doi: 10.4065/83.4.460 18380992.

33. Argenzio RA, Southworth M, Lowe JE, Stevens CE. Interrelationship of Na, HCO3, and volatile fatty acid transport by equine large intestine. The American journal of physiology. 1977;233(6):E469–78. doi: 10.1152/ajpendo.1977.233.6.E469 596440.

34. Holman DB, Chenier MR. Temporal changes and the effect of subtherapeutic concentrations of antibiotics in the gut microbiota of swine. FEMS microbiology ecology. 2014;90(3):599–608. doi: 10.1111/1574-6941.12419 25187398.

35. Al Jassim RA, Andrews FM. The bacterial community of the horse gastrointestinal tract and its relation to fermentative acidosis, laminitis, colic, and stomach ulcers. The Veterinary clinics of North America Equine practice. 2009;25(2):199–215. doi: 10.1016/j.cveq.2009.04.005 19580934.

36. Callaway TR, Dowd SE, Edrington TS, Anderson RC, Krueger N, Bauer N, et al. Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing. Journal of animal science. 2010;88(12):3977–83. doi: 10.2527/jas.2010-2900 20729286.

37. Dearing MD, Kohl KD. Beyond Fermentation: Other Important Services Provided to Endothermic Herbivores by their Gut Microbiota. Integrative and comparative biology. 2017;57(4):723–31. doi: 10.1093/icb/icx020 28662572.

38. Spence C, Wells WG, Smith CJ. Characterization of the primary starch utilization operon in the obligate anaerobe Bacteroides fragilis: Regulation by carbon source and oxygen. Journal of bacteriology. 2006;188(13):4663–72. doi: 10.1128/JB.00125-06 16788175; PubMed Central PMCID: PMC1482989.

39. Corzo G, Gilliland SE. Bile salt hydrolase activity of three strains of Lactobacillus acidophilus. Journal of dairy science. 1999;82(3):472–80. doi: 10.3168/jds.S0022-0302(99)75256-2 10194664.

40. Wood TM. Cellulase of Ruminococcus albus. Methods in Enzymology. 160: Academic Press; 1988. p. 216–21.

41. Patra AK, Yu Z. Essential oils affect populations of some rumen bacteria in vitro as revealed by microarray (RumenBactArray) analysis. Front Microbiol. 2015;6:297. doi: 10.3389/fmicb.2015.00297 25914694; PubMed Central PMCID: PMC4392297.

42. Zhao XH, Chen ZD, Zhou S, Song XZ, Ouyang KH, Pan K, et al. Effects of daidzein on performance, serum metabolites, nutrient digestibility, and fecal bacterial community in bull calves. Animal Feed Science and Technology. 2017;225:87–96. https://doi.org/10.1016/j.anifeedsci.2017.01.014.

43. Kristoffersen C, Jensen RB, Avershina E, Austbo D, Tauson AH, Rudi K. Diet-Dependent Modular Dynamic Interactions of the Equine Cecal Microbiota. Microbes and environments. 2016;31(4):378–86. doi: 10.1264/jsme2.ME16061 27773914; PubMed Central PMCID: PMC5158109.

44. Gruening P, Fulde M, Valentin-Weigand P, Goethe R. Structure, regulation, and putative function of the arginine deiminase system of Streptococcus suis. Journal of bacteriology. 2006;188(2):361–9. doi: 10.1128/JB.188.2.361-369.2006 16385025; PubMed Central PMCID: PMC1347268.

45. Alozie A, Koller K, Pose L, Raftis M, Steinhoff G, Westphal B, et al. Streptococcus bovis infectious endocarditis and occult gastrointestinal neoplasia: experience with 25 consecutive patients treated surgically. Gut pathogens. 2015;7:27. doi: 10.1186/s13099-015-0074-0 26473016; PubMed Central PMCID: PMC4607100.


Článek vyšel v časopise

PLOS One


2019 Číslo 12