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Applied Microbiology and Biotechnology

, Volume 103, Issue 1, pp 461–472 | Cite as

Heat stress mediates changes in fecal microbiome and functional pathways of laying hens

  • Lihui Zhu
  • Rongrong Liao
  • Ning Wu
  • Gensheng Zhu
  • Changsuo Yang
Environmental biotechnology

Abstract

Chicken gastrointestinal microbiota plays important roles in health, productivity, and disease. However, knowledge of the relationship between heat stress and the gut microbial ecosystem of poultry, especially laying hens, is still limited. Here, we aimed to provide important knowledge for heat stress intervention in the egg industry. We performed high-throughput sequencing metagenomics on fecal contents to unravel the microbial taxa and functional capacity of the gut microbiome of caged laying hens under heat stress. Results showed that the fecal microbial communities of laying hens were dominated by Firmicutes, Bacteroidetes, and Proteobacteria phyla. The Firmicutes were significantly decreased, and Bacteroidetes were increased in the fecal microbiota under heat stress. Functional prediction of these changes in microbiota revealed that metabolism-related pathways, including cysteine and methionine metabolism and benzoate degradation, were more abundant. Conversely, retinol metabolism and phenylpropanoid biosynthesis were decreased by heat stress, suggesting differences in metabolism between layers in different temperature environments. Clear contributions were identified between active taxa (genus level) and metabolic pathways, which were associated with the liver and intestinal dysfunction in layers. These data revealed that heat stress induced a significant taxonomic perturbation in the gut microbiome of caged laying hens. This was related to the negative effects of heat stress in poultry and provided important basic knowledge for heat stress intervention.

Keywords

Metagenome Microbial community Laying hens Heat stress Functional pathway 

Notes

Funding information

This study was supported by grants from the SAAS Program for Excellent Research Team (SPERT) and China Agriculture Research System (CARS-40-K03).

Compliance with ethical standards

This study was consistent with those approved by the Animal Ethics and Use Committee of Shanghai Academy of Agricultural Sciences that adopted the Animal Care and Use guidelines.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

253_2018_9465_MOESM1_ESM.pdf (357 kb)
ESM 1 (PDF 356 kb)

References

  1. Alhenaky A, Abdelqader A, Abuajamieh M, Al-Fataftah AR (2017) The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. J Therm Biol 70(Pt B):9–14.  https://doi.org/10.1016/j.jtherbio CrossRefPubMedGoogle Scholar
  2. Ammori BJ, Becker KL, Kite P, Snider RH, Nylen ES, White JC, Barclay GR, Larvin M, McMahon MJ (2003) Calcitonin precursors: early markers of gut barrier dysfunction in patients with acute pancreatitis. Pancreas 27(3):239–243CrossRefGoogle Scholar
  3. Andoh A, Nishida A, Takahashi K, Inatomi O, Imaeda H, Bamba S, Kito K, Sugimoto M, Kobayashi T (2016) Comparison of the gut microbial community between obese and lean peoples using 16S gene sequencing in a Japanese population. J Clin Biochem Nutr 59(1):65–70.  https://doi.org/10.3164/jcbn.15-152 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Awad E, Idrus Z, Soleimani AF, Jahromi MF (2018) Growth performance, duodenal morphology and the caecal microbial population in female broiler chickens fed glycine-fortified low protein diets under heat stress conditions. Br Poult Sci 59(3):340–348.  https://doi.org/10.1080/00071668.2018.1440377 CrossRefPubMedGoogle Scholar
  5. Ayala I, Martín Castillo A, Adánez G, Fernández-Rufete GPB, Castells MT (2009) Hyperlipidemic chicken as a model of non-alcoholic steatohepatitis. Exp Biol Med (Maywood) 234(1):10–16.  https://doi.org/10.3181/0807-RM-219 CrossRefGoogle Scholar
  6. Berk KA, Vongpromek R, Jiang M, Schneider WJ, Timman R, Verhoeven AJ, Bujo H, Sijbrands EJ, Mulder MT (2016) Levels of the soluble LDL receptor-relative LR11 decrease in overweight individuals with type 2 diabetes upon diet-induced weight loss. Atherosclerosis 254:67–72.  https://doi.org/10.1016/j.atherosclerosis.2016.09.066 CrossRefPubMedGoogle Scholar
  7. Bunchasak C (2009) Role of dietary methionine in poultry production. J Poult Sci 46(3):169–179CrossRefGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. D'Ambrosio DN, Clugston RD, Blaner WS (2011) Vitamin A metabolism: an update. Nutrients 3(1):63–103.  https://doi.org/10.3390/nu3010063 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Deeb N, Cahaner A (2002) Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. Poult Sci 81(3):293–301CrossRefGoogle Scholar
  11. Del Vesco AP, Gasparino E, Grieser DO, Zancanela V, Gasparin FR, Constantin J, Oliveira Neto AR (2014) Effects of methionine supplementation on the redox state of acute heat stress-exposed quails. J Anim Sci 92(2):806–815.  https://doi.org/10.2527/jas.2013-6829 CrossRefPubMedGoogle Scholar
  12. Del Vesco AP, Gasparino E, Grieser DO, Zancanela V, Voltolini DM, Khatlab AS, Guimarães SE, Soares MA, Oliveira Neto AR (2015) Effects of methionine supplementation on the expression of protein deposition-related genes in acute heat stress-exposed broilers. PLoS One 10(2):e0115821.  https://doi.org/10.1371/journal.pone.0115821 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Deng W, Dong XF, Tong JM, Zhang Q (2012) The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poult Sci 91(3):575–582.  https://doi.org/10.3382/ps.2010-01293 CrossRefPubMedGoogle Scholar
  14. Dewar ML, Arnould JP, Krause L, Dann P, Smith SC (2014) Interspecific variations in the faecal microbiota of Procellariiform seabirds. FEMS Microbiol Ecol 89(1):47–55.  https://doi.org/10.1111/1574-6941.12332 CrossRefPubMedGoogle Scholar
  15. Domingo MC, Yansouni C, Gaudreau C, Lamothe F, Lévesque S, Tremblay C, Garceau R (2015) Cloacibacillus sp., a potential human pathogen associated with Bacteremia in Quebec and new Brunswick. J Clin Microbiol 53(10):3380–3383.  https://doi.org/10.1128/JCM.01137-15 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Freestone PP, Sandrini SM, Haigh RD, Lyte M (2008) Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 16(2):55–64.  https://doi.org/10.1016/j.tim.2007.11.005 CrossRefPubMedGoogle Scholar
  17. Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Doré J, Henegar C, Rizkalla S, Clément K (2010) Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59(12):3049–3057.  https://doi.org/10.2337/db10-0253 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gagnière J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, Bringer MA, Pezet D, Bonnet M (2016) Gut microbiota imbalance and colorectal cancer. World J Gastroenterol 22(2):501–518.  https://doi.org/10.3748/wjg.v22.i2.501 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gu XH, Hao Y, Wang XL (2012) Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2. Intestinal oxidative stress. Poult Sci 91(4):790–799.  https://doi.org/10.3382/ps.2011-01628 CrossRefPubMedGoogle Scholar
  20. Gur TL, Bailey MT (2016) Effects of stress on commensal microbes and immune system activity. Adv Exp Med Biol 874:289–300.  https://doi.org/10.1007/978-3-319-20215-0_14 CrossRefPubMedGoogle Scholar
  21. Harte AL, da Silva NF, Creely SJ, McGee KC, Billyard T, Youssef-Elabd EM, Tripathi G, Ashour E, Abdalla MS, Sharada HM, Amin AI, Burt AD, Kumar S, Day CP, McTernan PG (2010) Elevated endotoxin levels in non-alcoholic fatty liver disease. J Inflamm (Lond) 7:15.  https://doi.org/10.1186/1476-9255-7-15 CrossRefGoogle Scholar
  22. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21(9):1552–1560.  https://doi.org/10.1101/gr.120618.111 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kim H, Kim DH, Seo KH, Chon JW, Nah SY, Bartley GE, Arvik T, Lipson R, Yokoyama W (2015) Modulation of the intestinal microbiota is associated with lower plasma cholesterol and weight gain in hamsters fed chardonnay grape seed flour. J Agric Food Chem 63(5):1460–1467.  https://doi.org/10.1021/jf5026373 CrossRefPubMedGoogle Scholar
  24. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, El-Omar EM, Brenner D, Fuchs CS, Meyerson M, Garrett WS (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14(2):207–215.  https://doi.org/10.1016/j.chom.2013.07.007 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lan PT, Sakamoto M, Benno Y (2004) Effects of two probiotic Lactobacillus strains on jejunal and cecal microbiota of broiler chicken under acute heat stress condition as revealed by molecular analysis of 16S rRNA genes. Microbiol Immunol 48(12):917–929CrossRefGoogle Scholar
  26. Lara LJ, Rostagno MH (2013) Impact of heat stress on poultry production. Animals (Basel) 3(2):356–369.  https://doi.org/10.3390/ani3020356 CrossRefGoogle Scholar
  27. Lewis JD, Chen EZ, Baldassano RN, Otley AR, Griffiths AM, Lee D, Bittinger K, Bailey A, Friedman ES, Hoffmann C, Albenberg L, Sinha R, Compher C, Gilroy E, Nessel L, Grant A, Chehoud C, Li H, Wu GD, Bushman FD (2015) Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn’s disease. Cell Host Microbe 18(4):489–500.  https://doi.org/10.1016/j.chom.2015.09.008 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Makovicky P, Dudova M, Tumova E, Rajmon R, Vodkova Z (2011) Experimental study of non-alcoholic fatty liver disease (NAFLD) on a model of starving chickens: is generalization of steatosis accompanied by fibrosis of the liver tissue? Pathol Res Pract 207(3):151–155.  https://doi.org/10.1016/j.prp.2010.12.002 CrossRefPubMedGoogle Scholar
  29. Mashaly MM, Hendricks GL, Kalama MA, Gehad AE, Abbas AO, Patterson PH (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci 83(6):889–894CrossRefGoogle Scholar
  30. Najafi P, Zulkifli I, Jajuli NA, Farjam AS, Ramiah SK, Amir AA, O'Reily E, Eckersall D (2015) Environmental temperature and stocking density effects on acute phase proteins, heat shock protein 70, circulating corticosterone and performance in broiler chickens. Int J Biometeorol 59(11):1577–1583.  https://doi.org/10.1007/s00484-015-0964-3 CrossRefPubMedGoogle Scholar
  31. Nicola S, Amoruso A, Deidda F, Pane M, Allesina S, Mogna L, Del Piano M, Mogna G (2016) Searching for the perfect homeostasis: five strains of Bifidobacterium longum from centenarians have a similar behavior in the production of cytokines. J Clin Gastroenterol 50:S126–S130CrossRefGoogle Scholar
  32. Patel T, Bhattacharya P, Das S (2016) Gut microbiota: an indicator to gastrointestinal tract diseases. J Gastrointest Cancer 47(3):232–238.  https://doi.org/10.1007/s12029-016-9820-x CrossRefPubMedGoogle Scholar
  33. Patrone V, Vajana E, Minuti A, Callegari ML, Federico A, Loguercio C, Dallio M, Tolone S, Docimo L, Morelli L (2016) Postoperative changes in fecal bacterial communities and fermentation products in obese patients undergoing bilio-intestinal bypass. Front Microbiol 7:200.  https://doi.org/10.3389/fmicb.2016.00200 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Peng Y, Leung HC, Yiu SM, Chin FY (2012) IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28(11):1420–1428.  https://doi.org/10.1093/bioinformatics/bts174 CrossRefPubMedGoogle Scholar
  35. Pokusaeva K, Fitzgerald GF, van Sinderen D (2011) Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6(3):285–306.  https://doi.org/10.1007/s12263-010-0206-6 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Renaudeau D, Collin A, Yahav S, de Basilio V, Gourdine JL, Collier RJ (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6(5):707–728.  https://doi.org/10.1017/S1751731111002448 CrossRefPubMedGoogle Scholar
  37. Scanlan PD, Shanahan F, O'Mahony C, Marchesi JR (2006) Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn’s disease. J Clin Microbiol 44:3980–3988.  https://doi.org/10.1128/JCM.00312-06 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Schirmer M, Franzosa EA, Lloyd-Price J, McIver LJ, Schwager R, Poon TW, Ananthakrishnan AN, Andrews E, Barron G, Lake K, Prasad M, Sauk J, Stevens B, Wilson RG, Braun J, Denson LA, Kugathasan S, McGovern DPB, Vlamakis H, Xavier RJ, Huttenhower C (2018) Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat Microbiol 3(3):337–346.  https://doi.org/10.1038/s41564-017-0089-z CrossRefPubMedPubMedCentralGoogle Scholar
  39. Serafini F, Strati F, Ruas-Madiedo P, Turroni F, Foroni E, Duranti S, Milano F, Perotti A, Viappiani A, Guglielmetti S, Buschini A, Margolles A, van Sinderen D, Ventura M (2013) Evaluation of adhesion properties and antibacterial activities of the infant gut commensal Bifidobacterium bifidum PRL2010. Anaerobe 21:9–17.  https://doi.org/10.1016/j.anaerobe.2013.03.003 CrossRefPubMedGoogle Scholar
  40. Settar P, Yalcin S, Turkmut L, Ozkan S, Cahanar A (1999) Season by genotype interaction related to broiler growth rate and heat tolerance. Poult Sci 78(10):1353–1358CrossRefGoogle Scholar
  41. Shini S, Bryden WL (2009) Occurrence and control of fatty liver haemorrhagic syndrome (FLHS) in caged hens. A report for the Australian Egg Corporation Limited AECL Publication No uq-105a AECL Project No UQ-105:1448–1316. Sydney, AustralianGoogle Scholar
  42. Sirisinha S (2015) The pleiotropic role of vitamin A in regulating mucosal immunity. Asian Pac J Allergy Immunol 33(2):71–89PubMedGoogle Scholar
  43. Sohail MU, Hume ME, Byrd JA, Nisbet DJ, Shabbir MZ, Ijaz A, Rehman H (2015) Molecular analysis of the caecal and tracheal microbiome of heat-stressed broilers supplemented with prebiotic and probiotic. Avian Pathol 44(2):67–74.  https://doi.org/10.1080/03079457.2015.1004622 CrossRefPubMedGoogle Scholar
  44. Sommer A (2008) Vitamin a deficiency and clinical disease: an historical overview. J Nutr 138(10):1835–1839CrossRefGoogle Scholar
  45. Song J, Xiao K, Ke YL, Jiao LF, Hu CH, Diao QY, Shi B, Zou XT (2014) Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poult Sci 93(3):581–588.  https://doi.org/10.3382/ps.2013-03455 CrossRefPubMedGoogle Scholar
  46. Sonnenburg JL, Bäckhed F (2016) Diet-microbiota interactions as moderators of human metabolism. Nature 535(7610):56–64.  https://doi.org/10.1038/nature18846 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Stanley D, Geier MS, Denman SE, Haring VR, Crowley TM, Hughes RJ, Moore RJ (2013) Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Vet Microbiol 164(1–2):85–92.  https://doi.org/10.1016/j.vetmic.2013.01.030 CrossRefPubMedGoogle Scholar
  48. Star L, Juul-Madsen HR, Decuypere E, Nieuwland MG, de Vries Reilingh G, van den Brand H, Kemp B, Parmentier HK (2009) Effect of early life thermal conditioning and immune challenge on thermotolerance and humoral immune competence in adult laying hens. Poult Sci 88(11):2253–2261.  https://doi.org/10.3382/ps.2008-00373 CrossRefPubMedGoogle Scholar
  49. Tsai MT, Chen YJ, Chen CY, Tsai MH, Han CL, Chen YJ, Mersmann HJ, Ding ST (2017) Identification of potential plasma biomarkers for nonalcoholic fatty liver disease by integrating transcriptomics and proteomics in laying hens. J Nutr 147(3):293–303.  https://doi.org/10.3945/jn.116.240358 CrossRefPubMedGoogle Scholar
  50. Verbrugghe E, Boyen F, Gaastra W, Bekhuis L, Leyman B, Van Parys A, Haesebrouck F, Pasmans F (2012) The complex interplay between stress and bacterial infections in animals. Vet Microbiol 155(2–4):115–127.  https://doi.org/10.1016/j.vetmic.2011.09.012 CrossRefPubMedGoogle Scholar
  51. Wang W, Chen L, Zhou R, Wang X, Song L, Huang S, Wang G, Xia B (2014) Increased proportions of Bifidobacterium and the Lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J Clin Microbiol 52(2):398–406.  https://doi.org/10.1128/JCM.01500-13 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wang W, Zheng S, Sharshov K, Sun H, Yang F, Wang X, Li L, Xiao Z (2016) Metagenomic profiling of gut microbial communities in both wild and artificially reared Bar-headed goose (Anser indicus). Microbiologyopen 6(2):e00429.  https://doi.org/10.1002/mbo3.429 CrossRefPubMedCentralGoogle Scholar
  53. 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 CrossRefPubMedGoogle Scholar
  54. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139:1844–1854.  https://doi.org/10.1053/j.gastro.2010.08.049 CrossRefPubMedGoogle Scholar
  55. Xu Y, Yang H, Zhang L, Su Y, Shi D, Xiao H, Tian Y (2016) High-throughput sequencing technology to reveal the composition and function of cecal microbiota in Dagu chicken. BMC Microbiol 16(1):259CrossRefGoogle Scholar
  56. Zhang M, Zou XT, Li H, Dong XY, Zhao W (2012) Effect of dietary γ-aminobutyric acid on laying performance, egg quality, immune activity and endocrine hormone in heat-stressed Roman hens. Anim Sci J 83(2):141–147.  https://doi.org/10.1111/j.1740-0929.2011.00939.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Animal Science and Veterinary MedicineShanghai Academy of Agricultural SciencesShanghaiChina
  2. 2.National Poultry Research Center for Engineering and TechnologyShanghaiChina
  3. 3.Shanghai Haifeng Dafeng Poultry Co., Ltd., Bright Food (Group) Co., Ltd.ShanghaiChina

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