Abstract
Infection with the nematode Haemonchus contortus causes host malnutrition and gastrointestinal injuries. The objective of this study was to investigate the effects of H. contortus infection on gastrointestinal contents of free amino acids (AA), the expression of AA transporters and microbiota with a focus on amino acid metabolism. Twenty-four Xiangdong black goats (13 ± 1.5 kg, 6 months old) were randomly assigned into the control group (n = 8) and the infected group (n = 16). The results showed that H. contortus infection increased (P < 0.05) the free AA contents in jejunum and ileum digesta. The concentrations of blood threonine, phenylalanine and tyrosine were lower (P < 0.05) in the infected group as compared to the control group. In the jejunum and ileum epithelium, H. contortus infection significantly (P < 0.05) down-regulated the expression of AA transporter b0,+AT/rBAT and B0AT1, but up-regulated (P < 0.05) the expression of transporter CAT2 and xCT. Furthermore, microbiota in both jejunum (Bifidobacteriaceae, Lachnospiraceae, Bacteroidaceae, Enterobacteriaceae, and Micrococcaceae) and ileum (Acidaminococcaceae, Desulfovibrionaceae, Bacteroidaceae, and Peptostreptococcaceae) were also altered at the family level by H. contortus infection. The commensal bacteria of jejunum showed a close correlation with amino acids, AA transporters, and amino acid metabolism, especially cystine. In conclusion, H. contortus infection affected the intestinal AA contents and the expression of intestinal AA transporters, suggesting altered AA metabolism and absorption, which were accompanied by changes in the relative abundances of gut bacteria that mediate amino acid metabolism.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- AA:
-
Amino acids
- GPCR:
-
G-protein-coupled receptor
- CaSR:
-
Calcium-sensing receptor
- mGluRs:
-
Metabotropic glutamate receptors
- T1R3:
-
Taste 1 receptor member 3
- GPRC6A:
-
G-protein-coupled receptor class C group 6 member A
- SLC:
-
Solute carrier
References
Adibi SA (1981) Peptide absorption and hydrolysis. Physiol Gastrointest Tract. 22(3):15–19
Al Bander Z, Nitert MD, Mousa A, Naderpoor N (2020) The gut microbiota and inflammation: an overview. Int J Env Res Pub He. 17(20):7618. https://doi.org/10.3390/ijerph17207618
Balic A, Bowles VM, Meeusen EN (2000) The immunobiology of gastrointestinal nematode infections in ruminants. Adv Parasitol 45:181–241. https://doi.org/10.1016/s0065-308x(00)45005-0
Balic A, Bowles VM, Meeusen EN (2002) Mechanisms of immunity to Haemonchus contortus infection in sheep. Parasite Immunol 24(1):39–46. https://doi.org/10.1046/j.0141-9838.2001.00432.x
Bambou JC, Arquet R, Archimede H, Alexandre G, Mandonnet N, Gonzalez-Garcia E (2009) Intake and digestibility of naive kids differing in genetic resistance and experimentally parasitized (indoors) with Haemonchus contortus in two successive challenges. J Anim Sci 87(7):2367–2375. https://doi.org/10.2527/jas.2008-1702
Bambou JC, Cei W, Camous S, Archimede H, Decherf A, Philibert L, Barbier C, Mandonnet N, Gonzalez-Garcia E (2013) Effects of single or trickle Haemonchus contortus experimental infection on digestibility and host responses of naive Creole kids reared indoor. Vet Parasitol 191(3–4):284–292. https://doi.org/10.1016/j.vetpar.2012.09.026
Bannai S (1986) Exchange of cystine and glutamate across plasma-membrane of human-fibroblasts. J Biol Chem 261(5):2256–2263
Barbot L, Windsor E, Rome S, Tricottet V, Reynes M, Topouchian A, Huneau JF, Gobert JG, Tome D, Kapel N (2003) Intestinal peptide transporter PepT1 is over-expressed during acute cryptosporidiosis in suckling rats as a result of both malnutrition and experimental parasite infection. Parasitol Res 89(5):364–370. https://doi.org/10.1007/s00436-002-0776-3
Bezencon C, le Coutre J, Damak S (2007) Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32(1):41–49. https://doi.org/10.1093/chemse/bjl034
Bezencon C, Fuerholz A, Raymond F, Mansourian R, Metairon S, Le Coutre J, Damak S (2008) Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J Comparat Neurol 509(5):514–525. https://doi.org/10.1002/cne.21768
Brestoff JR, Artis D (2013) Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 14(7):676–684. https://doi.org/10.1038/ni.2640
Broer S (2008) Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 88(1):249–286. https://doi.org/10.1152/physrev.00018.2006
Broer S, Fairweather SJ (2019) Amino acid transport across the mammalian intestine. Compr Physiol 9(1):343–373. https://doi.org/10.1002/cphy.c170041
Cantacessi C, Giacomin P, Croese J, Zakrzewski M, Sotillo J, McCann L, Nolan MJ, Mitreva M, Krause L, Loukas A (2014) Impact of experimental hookworm infection on the human gut microbiota. J Infect Dis 210(9):1431–1434. https://doi.org/10.1093/infdis/jiu256
Chen WX, Yan QX, Yang H, Zhou XL, Tan ZL (2019) Effects of restrictions on maternal feed intake on the immune indexes of umbilical cord blood and liver Toll-like receptor signaling pathways in fetal goats during pregnancy. J Anim Sci Biotechnol 10(1):29. https://doi.org/10.1186/s40104-019-0336-7
Claus SP, Tsang TM, Wang YL, Cloarec O, Skordi E, Martin FP, Rezzi S, Ross A, Kochhar S, Holmes E, Nicholson JK (2008) Systemic multicompartmental effects of the gut microbiome on mouse metabolic phenotypes. Mol Syst Biol. https://doi.org/10.1038/msb.2008.56
Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, Paris A, Want EJ, de Waziers I, Cloarec O, Richards SE, Wang Y, Dumas ME, Ross A, Rezzi S, Kochhar S, Van Bladeren P, Lindon JC, Holmes E, Nicholson JK (2011) Colonization-induced host-gut microbial metabolic interaction. Mbio. https://doi.org/10.1128/mBio.00271-10
Cortes A, Peachey L, Scotti R, Jenkins TP, Cantacessi C (2019) Helminth-microbiota cross-talk–A journey through the vertebrate digestive system. Mole Biochem Parasitol. 233:111222. https://doi.org/10.1016/j.molbiopara.2019.111222
D’Mello JF (2003) Amino acids in animal nutrition. CABI Publishing. https://doi.org/10.1079/97808519965470000
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38(6):685–688. https://doi.org/10.1038/s41587-020-0548-6
Duval D, Demangel C, Munierjolain K, Miossec S, Geahel I (1991) Factors controlling cell-proliferation and antibody-production in mouse hybridoma cells: 1 Influence of the amino-acid supply. Biotechnol Bioeng 38(6):561–570. https://doi.org/10.1002/bit.260380602
Else KJ, Finkelman FD, Maliszewski CR, Grencis RK (1994) Cytokine-mediated regulation of chronic intestinal helminth infection. J Experiment Med. 179(1):347–351. https://doi.org/10.1084/jem.179.1.347
Finkelman FD, Shea-Donohue T, Morris SC, Gildea L, Strait R, Madden KB, Schopf L, Urban JF Jr (2004) Interleukin-4-and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol Rev 201(1):139–155. https://doi.org/10.1111/j.0105-2896.2004.00192.x
Fons M, Cami B, Patte JC, Chippaux M (1987) Cloning in escherichia-coli of genes involved in the synthesis of proline and leucine in desulfovibrio-desulfuricans norway. Mol Gen Genet 206(1):141–143. https://doi.org/10.1007/Bf00326549
Gabriel AS, Uneyama H (2013) Amino acid sensing in the gastrointestinal tract. Amino Acids 45(3):451–461. https://doi.org/10.1007/s00726-012-1371-2
Gill HS (1994) Cell-mediated immunity in Merino lambs with genetic resistance to Haemonchus contortus. Intern J Parasitol. 24(5):749–756. https://doi.org/10.1016/0020-7519(94)90131-7
Guandalini S, Rubino A (1982) Development of dipeptide transport in the intestinal mucosa of rabbits. Pediatric Res 16(2):99–103. https://doi.org/10.1203/00006450-198202000-00004
Himukai M, Konno T, T J P r Hoshi, (1980) Age-dependent change in intestinal absorption of dipeptides and their constituent amino acids in the guinea pig. Pediatric Res 14(11):1272–1275. https://doi.org/10.1203/00006450-198011000-00024
Hofer D, Puschel B, Drenckhahn D (1996) Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. P Natl Acad Sci USA 93(13):6631–6634. https://doi.org/10.1073/pnas.93.13.6631
Holm JB, Sorobetea D, Kiilerich P, Ramayo-Caldas Y, Estelle J, Ma T, Madsen L, Kristiansen K, Svensson-Frej M (2015) Chronic trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of lactobacilli. PLoS ONE. https://doi.org/10.1371/journal.pone.0125495
Hoste H, Torres-Acosta JF, Paolini V, Aguilar-Caballero A, Etter E, Lefrileux Y, Chartier C, Broqua C (2005) Interactions between nutrition and gastrointestinal infections with parasitic nematodes in goats. Small Ruminant Res 60(1–2):141–151. https://doi.org/10.1016/j.smallrumres.2005.06.008
Howitt MR, Lavoie S, Michaud M, Blum AM, Tran SV, Weinstock JV, Gallini CA, Redding K, Margolskee RF, Osborne LC, Artis D, Garrett WS (2016) Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science 351(6279):1329–1333. https://doi.org/10.1126/science.aaf1648
International. A (2005) Official Methods of Analysis. 18th (ed). Assoc. Off. Anal. Chem. Int. Gaithersburg, MD.
Jenkins TP, Peachey LE, Ajami NJ, MacDonald AS, Hsieh MH, Brindley PJ, Cantacessi C, Rinaldi G (2018) Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota. Sci Rep 8(1):12072. https://doi.org/10.1038/s41598-018-30412-x
Jensen AN, Mejer H, Molbak L, Langkjaer M, Jensen TK, Angen O, Martinussen T, Klitgaard K, Baggesen DL, Thamsborg SM, Roepstorff A (2011) The effect of a diet with fructan-rich chicory roots on intestinal helminths and microbiota with special focus on Bifidobacteria and Campylobacter in piglets around weaning. Animal 5(6):851–860. https://doi.org/10.1017/S175173111000251x
Lacroux C, Nguyen TH, Andreoletti O, Prevot F, Grisez C, Bergeaud JP, Gruner L, Brunel JC, Francois D, Dorchies P, Jacquiet P (2006) Haemonchus contortus (Nematoda: Trichostrongylidae) infection in lambs elicits an unequivocal Th2 immune response. Vet Res 37(4):607–622. https://doi.org/10.1051/vetres:2006022
Lee SC, Tang MS, Lim YAL, Choy SH, Kurtz ZD, Cox LM, Gundra UM, Cho I, Bonneau R, Blaser MJ, Chua KH, Loke P (2014) Helminth colonization is associated with increased diversity of the gut microbiota. Plos Neglect Tropic Dis. 8(5):2880. https://doi.org/10.1371/journal.pntd.0002880
Lei WW, Ren WW, Ohmoto M, Urban JF, Matsumoto I, Margolskee RF, Jiang PH (2018) Activation of intestinal tuft cell-expressed Sucnr1 triggers type 2 immunity in the mouse small intestine. P Natl Acad Sci USA 115(21):5552–5557. https://doi.org/10.1073/pnas.1720758115
Levring TB, Hansen AK, Nielsen BL, Kongsbak M, von Essen MR, Woetmann A, Odum N, Bonefeld CM, Geisler C (2012) Activated human CD4(+) T cells express transporters for both cysteine and cystine. Sci Rep. https://doi.org/10.1038/srep00266
Li RW, Wu ST, Li WZ, Huang Y, Gasbarre LC (2011) Metagenome plasticity of the bovine abomasal microbiota in immune animals in response to ostertagia ostertagi infection. PLoS ONE. https://doi.org/10.1371/journal.pone.0024417
Li RW, Li WZ, Sun JJ, Yu P, Baldwin RL, Urban JF (2016) The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome. Sci Rep 6(1):1–10. https://doi.org/10.1038/srep20606
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Logue JB, Stedmon CA, Kellerman AM, Nielsen NJ, Andersson AF, Laudon H, Lindstrom ES, Kritzberg ES (2016) Experimental insights into the importance of aquatic bacterial community composition to the degradation of dissolved organic matter. Isme J 10(3):533–545. https://doi.org/10.1038/ismej.2015.131
Luo X-C, Chen Z-H, Xue J-B, Zhao D-X, Lu C, Li Y-H, Li S-M, Du Y-W, Liu Q, Wang P (2019) Infection by the parasitic helminth Trichinella spiralis activates a Tas2r-mediated signaling pathway in intestinal tuft cells. Proc Natl Acad Sci 116(12):5564–5569. https://doi.org/10.1073/pnas.1812901116
Macfarlane GT, Allison C, Gibson SAW, Cummings JH (1988) Contribution of the microflora to proteolysis in the human large-intestine. J Appl Bacteriol 64(1):37–46. https://doi.org/10.1111/j.1365-2672.1988.tb02427.x
Macfarlane GT, Cummings JH, Macfarlane S, Gibson GR (1989) Influence of retention time on degradation of pancreatic-enzymes by human colonic bacteria grown in a 3 stage continuous culture system. J Appl Bacteriol 67(5):521–527. https://doi.org/10.1111/j.1365-2672.1989.tb02524.x
MacLeod CL, Finley KD, Kakuda DK (1994) y (+)-type cationic amino acid transport: expression and regulation of the mCAT genes. J Exp Biol 196(1):109–121. https://doi.org/10.1242/jeb.196.1.109
Mamun MAA, Sandeman M, Rayment P, Brook-Carter P, Scholes E, Kasinadhuni N, Piedrafita D, Greenhill AR (2020) Variation in gut bacterial composition is associated with Haemonchus contortus parasite infection of sheep. Animal Microbiome 2:1–4. https://doi.org/10.1186/s42523-020-0021-3
Mao X, Zeng X, Qiao S, Wu G, Li D (2011) Specific roles of threonine in intestinal mucosal integrity and barrier function. Front Biosci (elite Ed) 3:1192–1200. https://doi.org/10.2741/e322
Matsumoto M, Kibe R, Ooga T, Aiba Y, Kurihara S, Sawaki E, Koga Y, Benno Y (2012) Impact of intestinal microbiota on intestinal luminal metabolome. Sci Rep 2:233. https://doi.org/10.1038/srep00233
McGinty JW, Ting H-A, Billipp TE, Nadjsombati MS, Khan DM, Barrett NA, Liang H-E, Matsumoto I, von Moltke J (2020) Tuft-cell-derived leukotrienes drive rapid anti-helminth immunity in the small intestine but are dispensable for anti-protist immunity. Immunity 52(3):528–541. https://doi.org/10.1016/j.immuni.2020.02.005
Miska KB, Fetterer RHJPS (2018) The effect of Eimeria maxima infection on the expression of amino acid and sugar transporters aminopeptidase, as well as the di-and tri-peptide transporter PepT1, is not solely due to decreased feed intake. Poultry Sci 97(5):1712–1721. https://doi.org/10.3382/ps/pey015
Miyamoto K, Shiraga T, Morita K, Yamamoto H, Haga H, Taketani Y, Tamai I, Sai Y, Tsuji A, Takeda E (1996) Sequence, tissue distribution and developmental changes in rat intestinal oligopeptide transporter. Biochimica Et Biophy Acta-Gene Structure Exp 1305(1–2):34–38. https://doi.org/10.1016/0167-4781(95)00208-1
Montagne L, Piel C, Lalles JP (2004) Effect of diet on mucin kinetics and composition: nutrition and health implications. Nutr Rev 62(3):105–114. https://doi.org/10.1301/nr.2004.mar.105-114
Morowitz MJ, Carlisle EM, Alverdy JC (2011) Contributions of intestinal bacteria to nutrition and metabolism in the critically ill. Surg Clin North Am 91(4):771–785. https://doi.org/10.1016/j.suc.2011.05.001
Nakamura E, Sato M, Yang HL, Miyagawa F, Harasaki M, Tomita K, Matsuoka S, Noma A, Iwai K, Minato N (1999) 4F2 (CD98) heavy chain is associated covalently with an amino acid transporter and controls intracellular trafficking and membrane topology of 4F2 heterodimer. J Biol Chem 274(5):3009–3016. https://doi.org/10.1074/jbc.274.5.3009
Nehra AK, Gowane GR, Kuriyal A, Chaurasiya A, Kumar R, Bhinsara DB, Parthasarathi BC, Bhawana K, Khare RK, Prasad A, Chandra D, Sankar M (2019) Immune response against subclinical haemonchosis in Himalayan hill goats. Vet Parasitol 267:47–53. https://doi.org/10.1016/j.vetpar.2019.01.005
Notter D, Andrew S, Zajac A (2003) Responses of hair and wool sheep to a single fixed dose of infective larvae of Haemonchus contortus. Small Ruminant Res 47(3):221–225. https://doi.org/10.1016/S0921-4488(02)00279-1
Palacin M, Nunes V, Font-Llitjos M, Jimenez-Vidal M, Fort J, Gasol E, Pineda M, Feliubadalo L, Chillaron J, Zorzano A (2005) The genetics of heteromeric amino acid transporters. Physiology 20:112–124. https://doi.org/10.1152/physiol.00051.2004
Pathak AK, Dutta N, Banerjee PS, Pattanaik AK, Sharma K (2013) Influence of dietary supplementation of condensed tannins through leaf meal mixture on intake, nutrient utilization and performance of haemonchus contortus infected sheep. Asian Austral J Anim 26(10):1446–1458. https://doi.org/10.5713/ajas.2013.13066
Ortega L, Quesada J, Ruiz A, Conde-Felipe MM, Ferrer O, Rodriguez F, Molina JM (2022) Local immune response of Canarian Majorera goats infected with Teladorsagia circumcincta. Parasites Vects. 15(1):25. https://doi.org/10.1186/s13071-021-05145-y
Reig N, Chillaron J, Bartoccioni P, Fernandez E, Bendahan A, Zorzano A, Kanner B, Palacin M, Bertran J (2002) The light subunit of system b(o,+) is fully functional in the absence of the heavy subunit. Embo J 21(18):4906–4914. https://doi.org/10.1093/emboj/cdf500
Schneeberger PHH, Coulibaly JT, Panic G, Daubenberger C, Gueuning M, Frey JE, Keiser J (2018) Investigations on the interplays between Schistosoma mansoni, praziquantel and the gut microbiome. Parasit Vectors 11(1):168. https://doi.org/10.1186/s13071-018-2739-2
Shakya K, Miller J, Horohov D (2009) A Th2 type of immune response is associated with increased resistance to Haemonchus contortus in naturally infected gulf coast native lambs. J Veterin Parasitol 163(1–2):57–66. https://doi.org/10.1016/j.vetpar.2009.03.052
Sivanand S, Vander Heiden MG (2020) Emerging roles for branched-chain amino acid metabolism in cancer. Cancer Cell 37(2):147–156. https://doi.org/10.1016/j.ccell.2019.12.011
Smith EL, Greene RD (1947) Further studies on the amino acid composition of immune proteins. J Biol Chem 171(1):355–362
Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S (2010) Myeloid-derived suppressor cells inhibit t-cell activation by depleting cystine and cysteine. Cancer Res 70(1):68–77. https://doi.org/10.1158/0008-5472.Can-09-2587
Tanaka H, Miyamoto K, Morita K, Haga H, Segawa H, Shiraga T, Fujioka A, Kouda T, Taketani Y, Hisano S, Fukui Y, Kitagawa K, Takeda E (1998) Regulation of the PepT1 peptide transporter in the rat small intestine in response to 5-fluorouracil-induced injury. Gastroenterology 114(4):714–723. https://doi.org/10.1016/s0016-5085(98)70585-2
Tsiagbe VK, Cook ME, Harper AE, Sunde ML (1987) Enhanced immune-responses in broiler chicks fed methionine-supplemented diets. Poult Sci 66(7):1147–1154. https://doi.org/10.3382/ps.0661147
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597
Whitt DD, Demoss RD (1975) Effect of microflora on the free amino acid distribution in various regions of the mouse gastrointestinal tract. Appl Microbiol 30(4):609–615. https://doi.org/10.1128/am.30.4.609-615.1975
Wlodarska M, Luo CW, Kolde R, d’Hennezel E, Annand JW, Heim CE, Krastel P, Schmitt EK, Omar AS, Creasey EA, Garner AL, Mohammadi S, O’Connell DJ, Abubucker S, Arthur TD, Franzosa EA, Huttenhower C, Murphy LO, Haiser HJ, Vlamakis H, Porter JA, Xavier RJ (2017) Indoleacrylic acid produced by commensal peptostreptococcus species suppresses inflammation. Cell Host Microbe 22(1):25. https://doi.org/10.1016/j.chom.2017.06.007
Wu J, Zhang XL, Tan ZL, Jiao JZ (2022) Distribution of free amino acids and mRNA expression of their corresponding transporters in the intestinal mucosa of goats feeding on a corn grain versus corn gluten diet. J Sci Food Agr 102(2):868–875. https://doi.org/10.1002/jsfa.11412
Xue MY, Xie YY,Zhong YF,Ma XJ, Sun HZ, Liu JX (2022) Integrated meta-omics reveals new ruminal microbial features associated with feed efficiency in dairy cattle. Microbiome 10(1):32. https://doi.org/10.1186/s40168-022-01228-9
Zhang MM, Gao C, Guo XT, Guo ST, Kang ZQ, Xiao D, Yan JX, Tao F, Zhang W, Dong WY, Liu P, Yang C, Ma CQ, Xu P (2018) Increased glutarate production by blocking the glutaryl-CoA dehydrogenation pathway and a catabolic pathway involving L-2-hydroxyglutarate. Nat Commun. https://doi.org/10.1038/s41467-018-04513-0
Zhang XM, Medrano RF, Wang M, Beauchemin KA, Ma ZY, Wang R, Wen JN, Bernard LA, Tan ZL (2019) Effects of urea plus nitrate pretreated rice straw and corn oil supplementation on fiber digestibility, nitrogen balance, rumen fermentation, microbiota and methane emissions in goats. J Anim Sci Biotechno. https://doi.org/10.1186/s40104-019-0312-2
Zhong RZ, Li HY, Fang Y, Sun HX, Zhou DW (2015) Effects of dietary supplementation with green tea polyphenols on digestion and meat quality in lambs infected with Haemonchus contortus. Meat Sci 105:1–7. https://doi.org/10.1016/j.meatsci.2015.02.003
Zhu X, Jiao J, Zhou C, Tang S, Wang M, Kang J, Han X, Tan Z (2018) Effects of dietary methionine and lysine supplementation on nutrients digestion, serum parameters and mRNA expression of related aminoacid sensing and transporting genes in growing goats. Small Ruminant Res 166:1–6. https://doi.org/10.1016/j.smallrumres.2018.07.002
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (Grants 31730092, 31972595), National Key R&D Program of China (2022YFD1301700) and Natural Science Foundation of Hunan Province (2020JJ5634).
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WC: data curation, methodology, validation, investigation, writing—original draft. QY: supervision, writing—original draft. RZ: conceptualization, methodology. ZT: resources, supervision, writing—review and editing.
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Chen, W., Yan, Q., Zhong, R. et al. Amino acid profiles, amino acid sensors and transporters expression and intestinal microbiota are differentially altered in goats infected with Haemonchus contortus. Amino Acids 55, 371–384 (2023). https://doi.org/10.1007/s00726-023-03235-y
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DOI: https://doi.org/10.1007/s00726-023-03235-y