Fungi in Gastrointestinal Tracts of Human and Mice: from Community to Functions

  • Jiayan Li
  • Daiwen Chen
  • Bing Yu
  • Jun He
  • Ping Zheng
  • Xiangbing Mao
  • Jie Yu
  • Junqiu Luo
  • Gang Tian
  • Zhiqing Huang
  • Yuheng Luo
Minireviews

Abstract

Fungi are often ignored in studies on gut microbes because of their low level of presence (making up only 0.1% of the total microorganisms) in the gastrointestinal tract (GIT) of monogastric animals. Recent studies using novel technologies such as next generation sequencing have expanded our understanding on the importance of intestinal fungi in humans and animals. Here, we provide a comprehensive review on the fungal community, the so-called mycobiome, and their functions from recent studies in humans and mice. In the GIT of humans, fungi belonging to the phyla Ascomycota, Basidiomycota and Chytridiomycota are predominant. The murine intestines harbor a more diverse assemblage of fungi. Diet is one of the major factors influencing colonization of fungi in the GIT. Presence of the genus Candida is positively associated with dietary carbohydrates, but are negatively correlated with dietary amino acids, proteins, and fatty acids. However, the relationship between diet and the fungal community (and functions), as well as the underlying mechanisms remains unclear. Dysbiosis of intestinal fungi can cause invasive infections and inflammatory bowel diseases (IBD). However, it is not clear whether dysbiosis of the mycobiome is a cause, or a result of IBD. Compared to non-inflamed intestinal mucosa, the abundance and diversity of fungi is significantly increased in the inflamed mucosa. The commonly observed commensal fungal species Candida albicans might contribute to occurrence and development of IBD. Limited studies show that Candida albicans might interact with immune cells of the host intestines through the pathways associated with Dectin-1, Toll-like receptor 2 (TLR2), and TLR4. This review is expected to provide new thoughts for future studies on intestinal fungi and for new therapies to fungal infections in the GIT of human and animals.

Keywords

Commensal fungi Community Diet Intestinal immune Candida albicans IBD 

References

  1. 1.
    Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904CrossRefPubMedGoogle Scholar
  2. 2.
    Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249CrossRefPubMedGoogle Scholar
  3. 3.
    Cerfbensussan N, Gaboriaurouthiau V (2010) The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 10:735–744CrossRefGoogle Scholar
  4. 4.
    Mao Y (2015) Role of gut microbiota in maternal glucose metabolism. Dissertation, University of Hong KongGoogle Scholar
  5. 5.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Arumugam M, Raes J, Pelletier E, Le PD, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM (2011) Enterotypes of the human gut microbiome. Nature 473:174–180CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Scupham AJ, Presley LL, Wei B, Bent E, Griffith N, Mcpherson M, Zhu F, Oluwadara O, Rao N, Braun J (2006) Abundant and diverse fungal microbiota in the murine intestine. Appl Environ Microbiol 72:793–801CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathology 87:888–891CrossRefPubMedGoogle Scholar
  9. 9.
    Soeta N, Terashima M, Gotoh M, Mori S, Nishiyama K, Ishioka K, Kaneko H, Suzutani T (2009) An improved rapid quantitative detection and identification method for a wide range of fungi. J Med Microbiol 58:1037–1044CrossRefPubMedGoogle Scholar
  10. 10.
    Valinsky L, Della VG, Jiang T, Borneman J (2002) Oligonucleotide fingerprinting of rRNA genes for analysis of fungal community composition. Appl Environ Microbiol 68:5999–6004CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Schoch CL, Consortium FB (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109:6241–6246CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Renaud M (2012) Role of gut microbiome-host metabolic interactions in metabolic diseases. Dissertation, Imperial College LondonGoogle Scholar
  13. 13.
    Fukuda S, Ohno H (2013) Gut microbiome and metabolic diseases. Semin Immunopathol 36:103–114CrossRefPubMedGoogle Scholar
  14. 14.
    Marteau P, Lepage P, Mangin I, Suau A, Doré J, Pochart P, Seksik P (2015) Gut flora and inflammatory bowel disease. Aliment Pharmacol Ther 20:18–23CrossRefGoogle Scholar
  15. 15.
    Loh G, Blaut M (2012) Role of commensal gut bacteria in inflammatory bowel diseases. Gut Microbes 3:544–555CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Ott SJ, Kühbacher T, Musfeldt M, Rosenstiel P, Hellmig S, Rehman A, Drews O, Weichert W, Timmis KN, Schreiber S (2008) Fungi and inflammatory bowel diseases: alterations of composition and diversity. Scand J Gastroenterol 43:831–841CrossRefPubMedGoogle Scholar
  17. 17.
    Iliev ID, Funari VA, Taylor KD, Nguyen Q, Reyes CN, Strom SP, Brown J, Becker CA, Fleshner PR, Dubinsky M (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336:1314–1317CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Ramaswamy K, Correa M, Koshy A (2007) Non-healing gastric ulcer associated with Candida infection. Indian J Med Microbiol 25:57–58CrossRefPubMedGoogle Scholar
  19. 19.
    Krause R, Reisinger EC (2005) Candida and antibiotic-associated diarrhoea. Clin Microbiol Infect 11:1–2CrossRefPubMedGoogle Scholar
  20. 20.
    Tong Y, Tang J (2017) Candida albicans infection and intestinal immunity. Microbiol Res 198:27–35CrossRefPubMedGoogle Scholar
  21. 21.
    Gosiewski T, Salamon D, Szopa M, Sroka A, Malecki MT, Bulanda M (2014) Quantitative evaluation of fungi of the genus Candida in the feces of adult patients with type 1 and 2 diabetes—a pilot study. Gut Pathog 6:43–47CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Sonoyama K, Miki A, Sugita R, Goto H, Nakata M, Yamaguchi N (2011) Gut colonization by Candida albicans aggravates inflammation in the gut and extra-gut tissues in mice. Med Mycol 49:237–247CrossRefPubMedGoogle Scholar
  23. 23.
    Suhr MJ, Hallenadams HE (2015) The human gut mycobiome: pitfalls and potentials—a mycologist’s perspective. Mycologia 107:1057–1073CrossRefPubMedGoogle Scholar
  24. 24.
    Schulze J, Sonnenborn U (2009) Yeasts in the gut: from commensals to infectious agents. Dtsch Arztebl Int 106:837–842PubMedPubMedCentralGoogle Scholar
  25. 25.
    Wheeler ML, Limon JJ, Underhill DM (2016) Immunity to commensal fungi: detente and disease. Annu Rev Pathol 12:359–385CrossRefPubMedGoogle Scholar
  26. 26.
    Hamad I, Sokhna C, Raoult D, Bittar F (2012) Molecular detection of eukaryotes in a single human stool sample from Senegal. PLoS One 7:561–567Google Scholar
  27. 27.
    Scanlan PD, Marchesi JR (2008) Micro-eukaryotic diversity of the human distal gut microbiota: qualitative assessment using culture-dependent and -independent analysis of faeces. ISME J 2:1183–1193CrossRefPubMedGoogle Scholar
  28. 28.
    Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75:583–609CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Koh AY (2013) Gastrointestinal colonization of fungi. Curr Fungal Infect Rep 7:144–151CrossRefGoogle Scholar
  30. 30.
    Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, GD W, Lewis JD, Bushman FD (2013) Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One 8:e66019CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Richard ML, Lamas B, Liguori G, Hoffmann TW, Sokol H (2014) Gut fungal microbiota: the Yin and Yang of inflammatory bowel disease. Inflamm Bowel Dis 21:656–665CrossRefGoogle Scholar
  32. 32.
    Mason KL, Downward JRE, Mason KD, Falkowski NR, Eaton KA, Kao JY, Young VB, Huffnagle GB (2012) Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy. Infect Immun 80:3371–3380CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Angebault C, Djossou F, Abélanet S, Permal E, Ben SM, Diancourt L, Bouchier C, Woerther PL, Catzeflis F, Andremont A (2013) Candida albicans is not always the preferential yeast colonizing humans: a study in Wayampi Amerindians. J Infect Dis 208:1705–1716CrossRefPubMedGoogle Scholar
  34. 34.
    Hallen-Adams HE, Kachman SD, Kim J, Legge RM, Martínez I (2015) Fungi inhabiting the healthy human gastrointestinal tract: a diverse and dynamic community. Fungal Ecol 15:9–17CrossRefGoogle Scholar
  35. 35.
    Dollive S, Chen YY, Grunberg S, Bittinger K, Hoffmann C, Vandivier L, Cuff C, Lewis JD, GD W, Bushman FD (2013) Fungi of the murine gut: episodic variation and proliferation during antibiotic treatment. PLoS One 8:e71806CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Gouba N, Raoult D, Drancourt M (2014) Eukaryote culturomics of the gut reveals new species. PLoS One 9:e106994CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Li Q, Wang C, Tang C, He Q, Li N, Li J (2014) Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn’s disease. J Clin Gastroenterol 48:513–523PubMedPubMedCentralGoogle Scholar
  38. 38.
    Pandey PK, Siddharth J, Verma P, Bavdekar A, Patole MS, Shouche YS (2012) Molecular typing of fecal eukaryotic microbiota of human infants and their respective mothers. J Biosci 37:221–226CrossRefPubMedGoogle Scholar
  39. 39.
    Ukhanova M, Wang X, Baer DJ, Novotny JA, Fredborg M, Mai V (2014) Effects of almond and pistachio consumption on gut microbiota composition in a randomised cross-over human feeding study. Br J Nutr 111:2146–2152CrossRefPubMedGoogle Scholar
  40. 40.
    Li Q, Wang C, Zhang Q, Tang C, Li N, Bing R, Li J (2012) Use of 18S ribosomal DNA polymerase chain reaction–denaturing gradient gel electrophoresis to study composition of fungal community in 2 patients with intestinal transplants. Hum Pathol 43:1273–1281CrossRefPubMedGoogle Scholar
  41. 41.
    Sokol H, Leducq V, Aschard H, et al. (2016) Fungal microbiota dysbiosis in IBD. Gut 66:1039–1048CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Biasoli MS, Tosello ME, Magaró HM (2002) Adherence of Candida strains isolated from the human gastrointestinal tract. Mycoses 45:465–469PubMedGoogle Scholar
  43. 43.
    Gouba N, Raoult D, Drancourt M (2014) Gut microeukaryotes during anorexia nervosa: a case report. BMC Res Notes 7:33–36CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Suhr MJ, Banjara N, Hallen-Adams HE (2015) Sequence-based methods for detecting and evaluating the human gut mycobiome. Lett Appl Microbiol 62:209–215CrossRefGoogle Scholar
  45. 45.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563CrossRefPubMedGoogle Scholar
  46. 46.
    Gouba N, Raoult D, Drancourt M (2013) Plant and fungal diversity in gut microbiota as revealed by molecular and culture investigations. PLoS One 8:e59474CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Penders J (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521CrossRefPubMedGoogle Scholar
  48. 48.
    Kong HH, Morris A (2017) The emerging importance and challenges of the human mycobiome. Virulence 8:310–312CrossRefPubMedGoogle Scholar
  49. 49.
    Suhr MJ, Banjara N, Hallen-Adams HE (2016) Sequence-based methods for detecting and evaluating the human gut mycobiome. Lett Appl Microbiol 62:209–215CrossRefPubMedGoogle Scholar
  50. 50.
    Rodríguez MM, Pérez D, Chaves FJ, Esteve E, Maringarcia P, Xifra G, Vendrell J, Jové M, Pamplona R, Ricart W (2016) Obesity changes the human gut mycobiome. Sci Rep 6:21679CrossRefGoogle Scholar
  51. 51.
    Zhang L, Mu C, He X, Yong S, Mao S, Jing Z, Smidt H, Zhu W (2016) Effects of dietary fibre source on microbiota composition in the large intestine of suckling piglets. FEMS Microbiol Lett 363:fnw138Google Scholar
  52. 52.
    Wang ZK, Yang YS, Stefka AT, Sun G, Peng LH (2014) Review article: fungal microbiota and digestive diseases. Aliment Pharmacol Ther 39:751–766CrossRefPubMedGoogle Scholar
  53. 53.
    Karkowska-Kuleta J, Kozik A (2015) Cell wall proteome of pathogenic fungi. Acta Biochim Pol 62:339–351CrossRefPubMedGoogle Scholar
  54. 54.
    Calich VL, Pina A, Felonato M, Bernardino S, Costa TA, Loures FV (2008) Toll-like receptors and fungal infections: the role of TLR2, TLR4 and MyD88 in paracoccidioidomycosis. FEMS Immunol Med Microbiol 53:1–7CrossRefPubMedGoogle Scholar
  55. 55.
    Gross O, Gewies A, Finger K, Schäfer M, Sparwasser T, Peschel C, Förster I, Ruland J (2006) Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 442:651–656CrossRefPubMedGoogle Scholar
  56. 56.
    Underhill DM, Iliev ID (2014) The mycobiota: interactions between commensal fungi and the host immune system. Nat Rev Immunol 14:405–416CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H, Haynes K, Steele C, Botto M, Gordon S (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8:31–38CrossRefPubMedGoogle Scholar
  58. 58.
    Netea MG, Brown GD, Kullberg BJ, Gow NA (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6:67–78CrossRefPubMedGoogle Scholar
  59. 59.
    Dillon S, Agrawal S, Banerjee K, Letterio J, Denning TL, Oswaldrichter K, Kasprowicz DJ, Kellar K, Pare J, Dyke TV (2006) Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest 116:916–928CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Romani L (2011) Immunity to fungal infections. Nat Rev Immunol 11:275–288CrossRefPubMedGoogle Scholar
  61. 61.
    Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, Venselaar H, Elbers CC, Johnson MD, Cambi A, Huysamen C (2009) Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 361:1760–1767CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Glocker EO, Hennigs A, Nabavi M, Woellner C, Salzer U, Pfeifer D, Veelken H, Warnatz K, Tahami F, Jamal S (2009) A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 361:1727–1735CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Mckenzie H, Main J, Pennington CR, Parratt D (1990) Antibody to selected strains of Saccharomyces cerevisiae (baker’s and brewer’s yeast) and Candida albicans in Crohn’s disease. Gut 31:536–538CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Colombel JF, Sendid B, Jouault T, Poulain D (2013) Secukinumab failure in Crohn’s disease: the yeast connection? Gut 62:800–801CrossRefPubMedGoogle Scholar
  65. 65.
    Qiu X, Zhang F, Yang X, Wu N, Jiang W, Li X, Li X, Liu Y (2015) Changes in the composition of intestinal fungi and their role in mice with dextran sulfate sodium-induced colitis. Sci Rep 5:10416CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Liguori G, Lamas B, Richard ML, Brandi G, Da CG, Hoffmann TW, Di SM, Calabrese C, Poggioli G, Langella P (2015) Fungal dysbiosis in mucosa-associated microbiota of Crohn’s disease patients. J Crohns Colitis 10:296–305CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Hoarau G, Mukherjee PK, Gower-Rousseau C, Hager C, Chandra J, Retuerto MA, Neut C, Vermeire S, Clemente J, Colombel JF (2016) Bacteriome and mycobiome interactions underscore microbial dysbiosis in familial Crohn’s disease. MBio 7:e01250–e01216CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Nakamura T, Yoshida M, Ishikawa H, Kameyama K, Wakabayashi G, Otani Y, Shimazu M, Tanabe M, Kawachi S, Kumai K (2007) Candida albicans aggravates duodenal ulcer perforation induced by administration of cysteamine in rats. J Gastroenterol Hepatol 22:749–756CrossRefPubMedGoogle Scholar
  69. 69.
    Chiaro TR, Soto R, Zac SW, Kubinak JL, Petersen C, Gogokhia L, Bell R, Delgado JC, Cox J, Voth W (2017) A member of the gut mycobiota modulates host purine metabolism exacerbating colitis in mice. Sci Transl Med 9:eaaf9044Google Scholar
  70. 70.
    Vautier S, Drummond RA, Chen K, Murray GI, Kadosh D, Brown AJ, Gow NA, Maccallum DM, Kolls JK, Brown GD (2015) Candida albicans colonization and dissemination from the murine gastrointestinal tract: the influence of morphology and Th17 immunity. Cell Microbiol 17:445–450CrossRefPubMedGoogle Scholar
  71. 71.
    Naglik JR, Moyes DL, Wächtler B, Hube B (2011) Candida albicans interactions with epithelial cells and mucosal immunity. Microbes Infect. 13:963–976CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Hooper LV, Dan RL, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336:1268–1273CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Günther Weindl JRN, Kaesler S, Biedermann T, Hube B, Korting HC, Schaller M (2008) Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J Clin Invest 117:3664–3672Google Scholar
  74. 74.
    Weindl G, Wagener J, Schaller M (2010) Epithelial cells and innate antifungal defense. J Dent Res 89:666–675CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Urban CF, Ermert D, Schmid M, Abuabed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5:e1000639CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Fl VDV, Marijnissen RJ, Kullberg BJ, Koenen HJ, Cheng SC, Joosten I, Wb VDB, Williams DL, Jw VDM, Joosten LA (2009) The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5:329–340CrossRefGoogle Scholar
  77. 77.
    Gringhuis SI, Wevers BA, Kaptein TM, van Capel TM, Theelen B, Boekhout T, de Jong EC, Geijtenbeek TB (2011) Selective C-Rel activation via Malt1 controls anti-fungal T(H)-17 immunity by dectin-1 and dectin-2. PLoS Pathog. 7:e1001259CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Moyes DL, Naglik JR (2011) Mucosal immunity and Candida albicans infection. Clin Dev Immunol 2011:346307Google Scholar
  79. 79.
    Zelante T, De LA, Bonifazi P, Montagnoli C, Bozza S, Moretti S, Belladonna ML, Vacca C, Conte C, Mosci P (2007) IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol 37:2695–2706CrossRefPubMedGoogle Scholar
  80. 80.
    Huang W, Na L, Fidel PL, Schwarzenberger P (2004) Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 190:624–631CrossRefPubMedGoogle Scholar
  81. 81.
    Y Z PAV, DM D YH, SM S QG, AR A ZM, N G FJD, WO (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14:282–289CrossRefGoogle Scholar
  82. 82.
    Luca AD, Zelante T, D'Angelo C, Zagarella S, Fallarino F, Spreca A, Iannitti RG, Bonifazi P, Renauld JC, Bistoni F (2010) IL-22 defines a novel immune pathway of antifungal resistance. Mucosal Immunol. 3:361–373CrossRefPubMedGoogle Scholar
  83. 83.
    Bai XD, Liu XH, Tong QY (2004) Intestinal colonization with Candida albicans and mucosal immunity. World J Gastroenterology 10:2124–2126CrossRefGoogle Scholar
  84. 84.
    Bujdáková H, Paulovicová E, Borecká-Melkusová S, Gasperík J, Kucharíková S, Kolecka A, Lell C, Jensen DB, Würzner R, Jr CD (2008) Antibody response to the 45 kDa Candida albicans antigen in an animal model and potential role of the antigen in adherence. J Med Microbiol 57:1466–1472CrossRefPubMedGoogle Scholar
  85. 85.
    Polonelli L, Ciociola T, Magliani W, Zanello PP, D'Adda T, Galati S, De BF, Arancia S, Gabrielli E, Pericolini E (2012) Peptides of the constant region of antibodies display fungicidal activity. PLoS One 7:e34105CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Jiayan Li
    • 1
  • Daiwen Chen
    • 1
  • Bing Yu
    • 1
  • Jun He
    • 1
  • Ping Zheng
    • 1
  • Xiangbing Mao
    • 1
  • Jie Yu
    • 1
  • Junqiu Luo
    • 1
  • Gang Tian
    • 1
  • Zhiqing Huang
    • 1
  • Yuheng Luo
    • 1
  1. 1.Key Laboratory for Animal Disease-Resistance Nutrition of China, Ministry of Education, Animal Nutrition InstituteSichuan Agricultural UniversityChengduChina

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