Cold stress changes the composition and function of microbiota in the content and mucosa of the ileum and colon in piglets
Shiyu Zhang A B , Yong Li A B , Jun Wang A B , Run Zhu A B , Lan Sun A B and Jiandui Mi A B C *A
B
C
Abstract
Cold stress is a significant factor that contributes to the imbalance of energy in piglets during their early life. Recent studies have shown that gut microbiota plays a crucial role in maintaining energy homeostasis under cold-stress conditions.
This study aims to investigate the effects of cold stress on the microbiota and expression pathways in the colon and ileum of weaned piglets, providing new insights and methods for helping piglets resist cold stress.
In total, 10 piglets in the cold-stress group (n = 5) and room-temperature group (n = 5) were sacrificed. Intestinal contents and mucosa samples were collected for 16S rRNA analysis.
The results showed that cold stress increased the observed features and chao1 index in the colonic mucosa. The beta diversity of ileum, colon and ileum mucosa was significantly changed. Under cold stress, the relative abundance of Acholeplasma, Proteiniphilum, and Olsenella increased in the contents of the ileum and colon. The relative abundance of Ruminococcaceae sp., Butyricicoccus, and Lachnospiraceae FCS020 increased in the mucosa of the colon. Sphingomonas, Helicobacter, Cutibacterium, and Bradyrhizobium were significantly increased in the mucosa of the ileum. In predicted functions, after cold stress, the purine metabolism and degradation increased in the content and mucosa of the ileum and mucosa of the colon. The fat biosynthesis pathway increased in the content of the colon. Complex carbohydrate degradation increased in the mucosa of both.
These findings suggest that cold stress has a significant impact on the species richness, composition, and predicted functions of the microbiota in the ileum and colon of piglets, with these effects varying depending on the location within the gut.
Therefore, we can help piglets resist cold stress by modifying the structure of gut microbiota through the addition of probiotics or adjusting the composition of their diet.
Keywords: cold stress, colon, content, gut microbiota, ileum, mucosa, weaned piglet, 16S rRNA.
References
Adams KL, Baker TH, Jensen AH (1980) Effect of supplemental heat for nursing piglets. Journal of Animal Science 50, 779-782.
| Crossref | Google Scholar | PubMed |
Azzouz D, Omarbekova A, Heguy A, Schwudke D, Gisch N, Rovin BH, Caricchio R, Buyon JP, Alekseyenko AV, Silverman GJ (2019) Lupus nephritis is linked to disease-activity associated expansions and immunity to a gut commensal. Annals of the Rheumatic Diseases 78, 947-956.
| Crossref | Google Scholar | PubMed |
Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, Eychmüller A, Gordts PLSM, Rinninger F, Bruegelmann K, Freund B, Nielsen P, Merkel M, Heeren J (2011) Brown adipose tissue activity controls triglyceride clearance. Nature Medicine 17, 200-205.
| Crossref | Google Scholar | PubMed |
Bin P, Tang Z, Liu S, Chen S, Xia Y, Liu J, Wu H, Zhu G (2018) Intestinal microbiota mediates Enterotoxigenic Escherichia coli-induced diarrhea in piglets. BMC Veterinary Research 14, 385.
| Crossref | Google Scholar | PubMed |
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu Y-X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, II, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, et al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852-857.
| Crossref | Google Scholar | PubMed |
Buffie CG, Pamer EG (2013) Microbiota-mediated colonization resistance against intestinal pathogens. Nature Reviews Immunology 13, 790-801.
| Crossref | Google Scholar | PubMed |
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581-583.
| Crossref | Google Scholar | PubMed |
Chen H, Mao X, He J, Yu B, Huang Z, Yu J, Zheng P, Chen D (2013) Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets. British Journal of Nutrition 110, 1837-1848.
| Crossref | Google Scholar | PubMed |
Chevalier C, Stojanović O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, Rigo D, Fabbiano S, Stevanovic A, Hagemann S, Montet X, Seimbille Y, Zamboni N, Hapfelmeier S, Trajkovski M (2015) Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 1360-1374.
| Crossref | Google Scholar | PubMed |
Chiang JYL, Ferrell JM (2020) Bile acid receptors FXR and TGR5 signaling in fatty liver diseases and therapy. American Journal of Physiology – Gastrointestinal and Liver Physiology 318, G554-G573.
| Crossref | Google Scholar | PubMed |
Chua H-H, Chou H-C, Tung Y-L, Chiang B-L, Liao C-C, Liu H-H, Ni Y-H (2018) Intestinal dysbiosis featuring abundance of Ruminococcus gnavus associates with allergic diseases in infants. Gastroenterology 154, 154-167.
| Crossref | Google Scholar | PubMed |
Davies LC, Rice CM, Palmieri EM, Taylor PR, Kuhns DB, McVicar DW (2017) Peritoneal tissue-resident macrophages are metabolically poised to engage microbes using tissue-niche fuels. Nature Communications 8, 2074.
| Crossref | Google Scholar | PubMed |
Dou S, Gadonna-Widehem P, Rome V, Hamoudi D, Rhazi L, Lakhal L, Larcher T, Bahi-Jaber N, Pinon-Quintana A, Guyonvarch A, Huërou-Luron ILE, Abdennebi-Najar L (2017) Characterisation of early-life fecal microbiota in susceptible and healthy pigs to post-weaning diarrhoea. PLoS ONE 12, e0169851.
| Crossref | Google Scholar | PubMed |
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nature Biotechnology 38, 685-688.
| Crossref | Google Scholar | PubMed |
Fan P, Liu P, Song P, Chen X, Ma X (2017) Moderate dietary protein restriction alters the composition of gut microbiota and improves ileal barrier function in adult pig model. Scientific Reports 7, 43412.
| Crossref | Google Scholar | PubMed |
Fouhse JM, Zijlstra RT, Willing BP (2016) The role of gut microbiota in the health and disease of pigs. Animal Frontiers 6, 30-36.
| Crossref | Google Scholar |
Funk I, Rimmel N, Schorsch C, Sieber V, Schmid J (2017) Production of dodecanedioic acid via biotransformation of low cost plant-oil derivatives using Candida tropicalis. Journal of Industrial Microbiology and Biotechnology 44, 1491-1502.
| Crossref | Google Scholar | PubMed |
Grala W, Buraczewska L, Wasilewko J, Verstegen MWA, Tamminga S, Jansman AJM, Huisman J, Korczyński W (1998) Flow of endogenous and exogenous nitrogen in different segments of the small intestine in pigs fed diets with soyabean concentrate, soyabean meal or rapeseed cake. Journal of Animal and Feed Sciences 7, 1-20.
| Crossref | Google Scholar |
Grefhorst A, van den Beukel JC, Dijk W, Steenbergen J, Voortman GJ, Leeuwenburgh S, Visser TJ, Kersten S, Friesema ECH, Themmen APN, Visser JA (2018) Multiple effects of cold exposure on livers of male mice. Journal of Endocrinology 238, 91-106.
| Crossref | Google Scholar | PubMed |
Gresse R, Chaucheyras-Durand F, Fleury MA, Van de Wiele T, Forano E, Blanquet-Diot S (2017) Gut microbiota dysbiosis in postweaning piglets: understanding the keys to health. Trends in Microbiology 25, 851-873.
| Crossref | Google Scholar | PubMed |
He W, Ding H, Feng Y, Liu X, Fang X, Gao F, Shi B (2024) Dietary-fat supplementation alleviates cold temperature-induced metabolic dysbiosis and barrier impairment by remodeling gut microbiota. Food & Function 15, 1443-1459.
| Crossref | Google Scholar | PubMed |
Henke MT, Kenny DJ, Cassilly CD, Vlamakis H, Xavier RJ, Clardy J (2019) Ruminococcus gnavus, a member of the human gut microbiome associated with Crohn’s disease, produces an inflammatory polysaccharide. Proceedings of the National Academy of Sciences of the United States of America 116, 12672-12677.
| Crossref | Google Scholar | PubMed |
Jo HE, Kwon M-S, Whon TW, Kim DW, Yun M, Lee J, Shin M-Y, Kim S-H, Choi H-J (2021) Alteration of gut microbiota after antibiotic exposure in finishing swine. Frontiers in Microbiology 12, 596002.
| Crossref | Google Scholar |
Joo S-Y, Park M-J, Kim K-H, Choi H-J, Chung T-W, Kim YJ, Kim JH, Kim K-J, Joo M, Ha K-T (2016) Cold stress aggravates inflammatory responses in an LPS-induced mouse model of acute lung injury. International Journal of Biometeorology 60, 1217-1225.
| Crossref | Google Scholar | PubMed |
Kamada N, Seo S-U, Chen GY, Núñez G (2013) Role of the gut microbiota in immunity and inflammatory disease. Nature Reviews Immunology 13, 321-335.
| Crossref | Google Scholar | PubMed |
Kaushik S, Kaur J (2005) Effect of chronic cold stress on intestinal epithelial cell proliferation and inflammation in rats. Stress 8, 191-197.
| Crossref | Google Scholar | PubMed |
Korhonen I (2006) Blood pressure and heart rate responses in men exposed to arm and leg cold pressor tests and whole-body cold exposure. International Journal of Circumpolar Health 65, 178-184.
| Crossref | Google Scholar | PubMed |
Li B, Li L, Li M, Lam SM, Wang G, Wu Y, Zhang H, Niu C, Zhang X, Liu X, Hambly C, Jin W, Shui G, Speakman JR (2019) Microbiota depletion impairs thermogenesis of brown adipose tissue and browning of white adipose tissue. Cell Reports 26, 2720-2737.e5.
| Crossref | Google Scholar | PubMed |
Liu H, Wang HH (2020) Impact of microbiota transplant on resistome of gut microbiota in gnotobiotic piglets and human subjects. Frontiers in Microbiology 11, 932.
| Crossref | Google Scholar | PubMed |
Mazzoli R, Pessione E (2016) The neuro-endocrinological role of microbial glutamate and GABA signaling. Frontiers in Microbiology 7, 1934.
| Crossref | Google Scholar | PubMed |
Merrifield CA, Lewis MC, Berger B, Cloarec O, Heinzmann SS, Charton F, Krause L, Levin NS, Duncker S, Mercenier A, Holmes E, Bailey M, Nicholson JK (2016) Neonatal environment exerts a sustained influence on the development of the intestinal microbiota and metabolic phenotype. The ISME Journal 10, 145-157.
| Crossref | Google Scholar | PubMed |
Moreno-Navarrete JM, Fernandez-Real JM (2019) The gut microbiota modulates both browning of white adipose tissue and the activity of brown adipose tissue. Reviews in Endocrine and Metabolic Disorders 20, 387-397.
| Crossref | Google Scholar | PubMed |
Mulder IE, Schmidt B, Stokes CR, Lewis M, Bailey M, Aminov RI, Prosser JI, Gill BP, Pluske JR, Mayer C-D, Musk CC, Kelly D (2009) Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology 7, 79.
| Crossref | Google Scholar | PubMed |
Obeng N, Bansept F, Sieber M, Traulsen A, Schulenburg H (2021) Evolution of microbiota-host associations: the microbe’s perspective. Trends in Microbiology 29, 779-787.
| Crossref | Google Scholar | PubMed |
Pang J, Liu Y, Kang L, Ye H, Zang J, Wang J, Han D (2022) Bifidobacterium animalis promotes the growth of weaning piglets by improving intestinal development, enhancing antioxidant capacity, and modulating gut microbiota. Applied and Environmental Microbiology 88, e01296-22.
| Crossref | Google Scholar |
Qi R, Zhang Z, Wang J, Qiu X, Wang Q, Yang F, Huang J, Liu Z (2021) Introduction of colonic and fecal microbiota from an adult pig differently affects the growth, gut health, intestinal microbiota and blood metabolome of newborn piglets. Frontiers in Microbiology 12, 623673.
| Crossref | Google Scholar |
Qin W, Xu B, Chen Y, Yang W, Xu Y, Huang J, Duo T, Mao Y, Zhou G, Yan X, Ma L (2022) Dietary ellagic acid supplementation attenuates intestinal damage and oxidative stress by regulating gut microbiota in weanling piglets. Animal Nutrition 11, 322-333.
| Crossref | Google Scholar | PubMed |
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biology 12, R60.
| Crossref | Google Scholar | PubMed |
Swiergiel AH (1987) Decrease in body temperature and locomotor activity as an adaptational response in piglets exposed to cold on restricted feeding. Physiology & Behavior 40, 117-125.
| Crossref | Google Scholar | PubMed |
Tan Z, Dong W, Ding Y, Ding X, Zhang Q, Jiang L (2019) Changes in cecal microbiota community of suckling piglets infected with porcine epidemic diarrhea virus. PLoS ONE 14, e0219868.
| Crossref | Google Scholar |
Tang S, Zhang S, Zhong R, Su D, Xia B, Liu L, Chen L, Zhang H (2021) Time-course alterations of gut microbiota and short-chain fatty acids after short-term lincomycin exposure in young swine. Applied Microbiology and Biotechnology 105, 8441-8456.
| Crossref | Google Scholar | PubMed |
Tao X, Xu Z, Wan J (2015) Intestinal microbiota diversity and expression of pattern recognition receptors in newly weaned piglets. Anaerobe 32, 51-56.
| Crossref | Google Scholar | PubMed |
Tauqir NA (2017) Absorption and transportation of amino acids in animals: a review. Journal of Environmental and Agricultural Sciences 9, 96-109 Available at https://www.agropublishers.com/files/JEAS-09-96-109_amino_acid_review1.PDF.
| Google Scholar |
Thong HT, Liebert F (2004) Amino acid requirement of growing pigs depending on amino acid efficiency and level of protein deposition 1st communication: lysine. Archives of Animal Nutrition 58, 69-87.
| Crossref | Google Scholar | PubMed |
van der Wielen N, Moughan PJ, Mensink M (2017) Amino acid absorption in the large intestine of humans and porcine models. The Journal of Nutrition 147, 1493-1498.
| Crossref | Google Scholar | PubMed |
Wang S, Xing Y, Xu Y, Chen K, Ali Q, Ullah M, Sun Z (2018) In vivo endothelial cell-specific expression of AMPKα attenuates cold-induced pulmonary vascular dysfunction and hypertension by mitigating inflammation. The FASEB Journal 32, 845.9.
| Crossref | Google Scholar |
Wei X, Tsai T, Howe S, Zhao J (2021) Weaning induced gut dysfunction and nutritional interventions in nursery pigs: a partial review. Animals 11, 1279.
| Crossref | Google Scholar |
Wu Q, Liang X, Wang K, Lin J, Wang X, Wang P, Zhang Y, Nie Q, Liu H, Zhang Z, Liu J, Pang Y, Jiang C (2021) Intestinal hypoxia-inducible factor 2α regulates lactate levels to shape the gut microbiome and alter thermogenesis. Cell Metabolism 33, 1988-2003.e7.
| Crossref | Google Scholar | PubMed |
Xu Z, Chen W, Wang L, Zhou Y, Nong Q, Valencak TG, Wang Y, Xie J, Shan T (2021) Cold exposure affects lipid metabolism, fatty acids composition and transcription in pig skeletal muscle. Frontiers in Physiology 12, 748801.
| Crossref | Google Scholar | PubMed |
Yin J, Han H, Li Y, Liu Z, Zhao Y, Fang R, Huang X, Zheng J, Ren W, Wu F, Liu G, Wu X, Wang K, Sun L, Li C, Li T, Yin Y (2018) Lysine restriction affects feed intake and amino acid metabolism via gut microbiome in piglets. Cellular Physiology and Biochemistry 44, 1749-1761.
| Crossref | Google Scholar | PubMed |
Zhang M, Gao C, Guo X, Guo S, Kang Z, Xiao D, Yan J, Tao F, Zhang W, Dong W, Liu P, Yang C, Ma C, Xu P (2018) Increased glutarate production by blocking the glutaryl-CoA dehydrogenation pathway and a catabolic pathway involving L-2-hydroxyglutarate. Nature Communications 9, 2114.
| Crossref | Google Scholar | PubMed |
Zhang Z, Li Z, Zhao H, Chen X, Tian G, Liu G, Cai J, Jia G (2020) Effects of drinking water temperature and flow rate during cold season on growth performance, nutrient digestibility and cecum microflora of weaned piglets. Animals 10, 1048.
| Crossref | Google Scholar |
Zhang Y, Sun L, Zhu R, Zhang S, Liu S, Wang Y, Wu Y, Xing S, Liao X, Mi J (2022a) Porcine gut microbiota in mediating host metabolic adaptation to cold stress. npj Biofilms and Microbiomes 8, 18.
| Crossref | Google Scholar | PubMed |
Zhang Y, Gan Y, Wang J, Feng Z, Zhong Z, Bao H, Xiong Q, Wang R (2022b) Dysbiosis of gut microbiota and intestinal barrier dysfunction in pigs with pulmonary inflammation induced by Mycoplasma hyorhinis infection. mSystems 7, e00282-22.
| Crossref | Google Scholar |
Zheng H, Liang H, Wang Y, Miao M, Shi T, Yang F, Liu E, Yuan W, Ji Z-S, Li D-K (2016) Altered gut microbiota composition associated with eczema in infants. PLoS ONE 11, e0166026.
| Crossref | Google Scholar | PubMed |
Zheng Q, Lin J, Huang J, Zhang H, Zhang R, Zhang X, Cao C, Hambly C, Qin G, Yao J, Song R, Jia Q, Wang X, Li Y, Zhang N, Piao Z, Ye R, Speakman JR, Wang H, Zhou Q, Wang Y, Jin W, Zhao J (2017) Reconstitution of UCP1 using CRISPR/Cas9 in the white adipose tissue of pigs decreases fat deposition and improves thermogenic capacity. Proceedings of the National Academy of Sciences 114, E9474-E9482.
| Crossref | Google Scholar |
Zhou X, Liu Y, Xiong X, Chen J, Tang W, He L, Zhang Z, Yin Y, Li F (2022) Intestinal accumulation of microbiota-produced succinate caused by loss of microRNAs leads to diarrhea in weanling piglets. Gut Microbes 14, 2091369.
| Crossref | Google Scholar | PubMed |
Ziętak M, Kovatcheva-Datchary P, Markiewicz LH, Ståhlman M, Kozak LP, Bäckhed F (2016) Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metabolism 23, 1216-1223.
| Crossref | Google Scholar | PubMed |
Zivkovic AM, German JB, Lebrilla CB, Mills DA (2011) Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proceedings of the National Academy of Sciences of the United States of America 108, 4653-4658.
| Crossref | Google Scholar | PubMed |
Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC, Troost FJ, Bork P, Wels M, de Vos WM, Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. The ISME Journal 6, 1415-1426.
| Crossref | Google Scholar | PubMed |
Zolotova NA, Dzhalilova DS, Khochanskiy DN, Tsvetkov IS, Kosyreva AM, Ponomarenko EA, Diatroptova MA, Mikhailova LP, Mkhitarov VA, Makarova OV (2021) Morphofunctional changes in colon after cold stress in male C57BL/6 mice susceptible and tolerant to hypoxia. Bulletin of Experimental Biology and Medicine 171, 499-503.
| Crossref | Google Scholar | PubMed |