Skip to main content

Advertisement

SpringerLink
Log in

Bamboo nutrients and microbiome affect gut microbiome of giant panda

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

To investigate the relationship between the bamboo including its nutrients and microbiome, and gut microbiome of giant panda, different bamboo species were provided for feeding the giant pandas. Nutrients of bamboo were examined, and the bamboo microbiome and gut microbiome of giant panda were investigated using high throughput sequencing. The results revealed that the composition of gut microbiome in giant panda varied among groups with different bamboo diet. Except for fat and hemicellulose, cellulose, lignin, carbohydrate, protein, flavone and tannin were significantly different between different bamboo species (p < 0.05). PCoA showed that the composition of bamboo microbiome varied by different species. Significant differences in richness and diversity of bacteria were observed between different bamboo (p < 0.05), as well as the abundance of the main bacteria and fungi at phylum and genus level (Kruskal-Wallis, LDA > 4). Interestingly, the content of lignin and cellulose in bamboo was positively associated with the relative abundance of Streptococcus and Clostridium in gut of giant panda, respectively (p < 0.05). The diversity of bamboo bacteria was positively correlated with that of gut bacteria in giant panda (p < 0.05). Significant associations of certain bacteria and fungi between bamboo and gut of giant panda (p < 0.05) were found. 36 bacterial and 54 fungal genera were both shared between bamboo and the gut of giant panda in all groups. Our results demonstrated that the gut microbial community varied between giant pandas fed on different bamboo species revealing that bamboo nutrients and microbiome affect gut microbiome of giant panda. Our findings contributed to the deeper understanding of dietary or environmental impact on gut microbiome of giant panda.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akinoso R, Aboaba S, Olajide W (2012) Optimization of roasting temperature and time during oil extraction from orange ( Citrus sinensis ) seeds: a response surface methodology approach. Afr J Food Agric Nutri Develop 11(6):5300–5317

  • Arzanlou M, Groenewald JZ, Gams W, Braun U, Shin HD, Crous PW (2007) Phylogenetic and morphotaxonomic revision of Ramichloridium and allied genera. Stud Mycol 58:57–93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aveskamp MM, Gruyter CPW (2008) Biology and recent developments in the systematics of Phoma, a complex genus of major quarantine significance. Fungal Divers 31:1–18

    Google Scholar 

  • Bäckhed F, Ding H, Wang T, Hooper LV, Gou YK, Nagy A et al (2004) The gut microbiome as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101:15718–15723

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatchevadatchary P et al (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17:690–703

    Article  PubMed  CAS  Google Scholar 

  • Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Rob K, Gregory J, C et al (2014) Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett 17:979–987

  • Borody TJ, Alexander K (2012) Fecal microbiome transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 9:88–96

    Article  CAS  Google Scholar 

  • Bowers RM, Nicholas C, Emerson JB, Christine W, Hannigan MP, Noah F (2013) Seasonal variability in bacterial and fungal diversity of the near-surface atmosphere. Environ Sci Tech 47:12097

  • Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C, Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354–369

    Article  PubMed  CAS  Google Scholar 

  • Bremner JM, Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN et al (1996) Nitrogen - total. In: Sparks D et al (eds) In methods ofsoil analysis. Part 3: chemical methods, Madison, Soil ScienceSociety of America and American Society of Agronomy, pp 1085–1123

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight RJ (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4156–4122

  • Carlotta DF, Duccio C, Monica DP, Matteo R, Jean Baptiste P, Sebastien M et al (2010) Impact of diet in shaping gut microbiome revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107:14691–14696

    Article  Google Scholar 

  • Chen D, Li C, Feng L, Zhang Z, Zhang H, Cheng G, Li D, Zhang G, Wang H, Chen Y, Feng M, Wang C, Wu H, Deng L, Ming H, Yang X (2018) Analysis of the influence of living environment and age on vaginal fungal microbiome in giant pandas (Ailuropoda melanoleuca) by high throughput sequencing. Microb Pathog 115:280–286

    Article  PubMed  Google Scholar 

  • Christian H, Serena D, Stephanie G, Jun C, Hongzhe L, W. G D et al (2013) Archaea and Fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One 8:e66019

    Article  CAS  Google Scholar 

  • Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O'Sullivan O, Fitzgerald GF, Deane J, O'Connor M, Harnedy N, O'Connor K, O'Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O'Toole PW (2012) Gut microbiome composition correlates with diet and health in the elderly. Nature 488:178–184

    Article  PubMed  CAS  Google Scholar 

  • Dang P, Yu X, Le H, Liu J, Shen Z, Zhao Z (2017) Effects of stand age and soil properties on soil bacterial and fungal community composition in Chinese pine plantations on the loess plateau. PLoS One 12:e0186501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daniel H, Gholami AM, Berry D, Desmarchelier C, Hahne H, Loh G, Mondot S, Lepage P, Rothballer M, Walker A, Böhm C, Wenning M, Wagner M, Blaut M, Schmitt-Kopplin P, Kuster B, Haller D, Clavel T (2014) High-fat diet alters gut microbiome physiology in mice. ISME J 8:295–308

    Article  PubMed  CAS  Google Scholar 

  • Deng YJ, Wang SY (2016) Synergistic growth in bacteria depends on substrate complexity. J Microbiol 54:23–30

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate. OTU sequences from microbial amplicon reads. Nat Meth 10(10):996–998

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang Z, Smith RL Jr (2016). Production of biofuels and chemicals from lignin

  • Frese S. A, Parker K, Calvert C. C, Mills D. A (2015). Diet shapes the gut microbiome of pigs during nursing and weaning. Microbiome,3,1(2015-07-01)3: 28

  • Guo M, Chen J, Li Q, Fu Y, Fan G, Ma J et al (2018) Dynamics of gut microbiome in Giant panda cubs reveal transitional microbes and pathways in early life. Front Microbiol 9:3138

    Article  PubMed  PubMed Central  Google Scholar 

  • Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis T, Human Microbiome Consortium, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han J, Xia D, Li L, Lei S, Kai Y, Zhang L (2009) Diversity of Culturable Bacteria isolated from root domains of Moso bamboo (Phyllostachys edulis). Microb Ecol 58:363–373

    Article  PubMed  Google Scholar 

  • Hannula SE, Zhu F, Heinen R (2019) Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nat Commun 10:1254

  • Helander M, Huitu O, Sieber TN, Jia J, Niemelä P, Saikkonen K (2013) Endophytic fungi and silica content of different bamboo species in giant panda diet. Symbiosis 61:13–22

    Article  CAS  Google Scholar 

  • Hildebrandt M. A, Hoffmann C, Sherrill-Mix S. A, Keilbaugh S. A, Hamady M, Chen Y. Y et al (2009). High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology137: 1716-1724.e1711-1712

  • Hu Y, Wu Q, Ma S, Ma T, Shan L, Wang X, Nie Y, Ning Z, Yan L, Xiu Y, Wei F (2017) Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc Natl Acad Sci U S A 114:1081–1086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang X, Liu L, Wen T, Zhu R, Zhang J, Cai Z (2015) Illumina MiSeq investigations on the changes of microbial community in the Fusarium oxysporum f.sp. cubense infected soil during and after reductive soil disinfestation. Microbiol Res 181:33–42

    Article  PubMed  CAS  Google Scholar 

  • International AOAC (1995). Official methods of analysis of AOAC international, 16th edition. Volume 1

  • Jain A, Xin HL, Wei NC (2018) Similarities and differences in gut microbiome composition correlate with dietary patterns of Indian and Chinese adults. AMB Express 8:104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiménez DJ, Chavesmoreno D, Elsas JDV (2015) Unveiling the metabolic potential of two soil-derived microbial consortia selected on wheat straw. Sci Rep 5:1–17

    Google Scholar 

  • Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  CAS  Google Scholar 

  • Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, Dermody TS, Pfeiffer JK (2011) Intestinal microbiome promote enteric virus replication and systemic pathogenesis. Science 334:249–252

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larsen OFA, Claassen E (2018) The mechanistic link between health and gut microbiome diversity. Sci Rep 8:2183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li R, Fan W, Tian G, Zhu H, He L, Cai J et al (2010) The sequence and de novo assembly of the Giant panda genome. Nature 463:311

    Article  PubMed  CAS  Google Scholar 

  • Lifeng Z, Qi W, Jiayin D, Shanning Z, Fuwen W (2011) Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci U S A 108:17714–17719

    Article  Google Scholar 

  • Liu X, Wang T, Wang T, Skidmore AK, Songer M (2015) How do two giant panda populations adapt to their habitats in the Qinling and Qionglai Mountains, China. Environ Sci Pollut Res 22:1175–1185

    Article  Google Scholar 

  • Liu Y, Zachow C, Raaijmakers JM, De BI (2016) Elucidating the diversity of aquatic Microdochium and Trichoderma species and their activity against the fish pathogen Saprolegnia diclina. Int J Mol Sci 17:140

    Article  PubMed Central  CAS  Google Scholar 

  • Liu H, Zhang C, Liu Y, Duan H (2019) Total flavonoid contents in bamboo diets and reproductive hormones in captive pandas: exploring the potential effects on the female giant panda (Ailuropoda melanoleuca). Conservation physiology7:coy068

    Article  PubMed  PubMed Central  Google Scholar 

  • Maurice CF, Knowles SC, Ladau J, Pollard KS, Fenton A, Pedersen AB, Turnbaugh PJ (2015) Marked seasonal variation in the wild mouse gut microbiome. ISME J 9:2423–2434

    Article  PubMed  CAS  Google Scholar 

  • Michl SC, Ratten JM, Beyer M, Hasler M, Laroche J, Schulz C (2017) The malleable gut microbiome of juvenile rainbow trout (Oncorhynchus mykiss): diet-dependent shifts of bacterial community structures. PLoS One 12:e0177735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Montagne L, Pluske JR, Hampson DJ (2003) A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals [review]. Animal Feed Science & Technology 108:95–117

    Article  Google Scholar 

  • Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG (2015) The infant microbiome development: mom matters. Trends Mol Med 21:109–117

    Article  PubMed  Google Scholar 

  • Nelson TM, Rogers TL, Carlini AR, Brown MV (2013) Diet and phylogeny shape the gut microbiome of Antarctic seals: a comparison of wild and captive animals. Environ Microbiol 15:1132–1145

    Article  PubMed  CAS  Google Scholar 

  • Nicholson JK, Elaine H, James K, Remy B, Glenn G, Wei J et al (2012) Host-gut microbiome metabolic interactions. Science 336:1262–1267

    Article  PubMed  CAS  Google Scholar 

  • Persson IL, Wikan S, Swenson JE, Mysterud I (2001) The diet of the brown bear Ursus arctos in the Pasvik Valley northeastern Norway. Wildl Biol 7:27–37

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  PubMed  CAS  Google Scholar 

  • Rondel C, Marcato-Romain CE, Girbal-Neuhauser E (2013) Development and validation of a colorimetric assay for simultaneous quantification of neutral and uronic sugars. Water Res 47:2901–2908

    Article  PubMed  CAS  Google Scholar 

  • Sarı FN, Dizdar EA, Oguz S, Erdeve O, Uras N, Dilmen U (2010) Oral probiotics: Lactobacillus sporogenes for prevention of necrotizing enterocolitis in very low-birth weight infants: a randomized, controlled trial. Eur J Clin Nutr 86:S87–S87

    Google Scholar 

  • Schaller GB, Hu JC, Pan WS, Zhu J (1985) The giant panda of Wolong. University of Chicago Press, Chicago

  • Schmidt E, Mykytczuk N, Schulte-Hostedde AI (2019) Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME J 13:1293–1305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiome. Pharmacol Res 69:52–60

    Article  PubMed  CAS  Google Scholar 

  • Shengzhi Y, Xin G, Meng J, Zhang A, Zhou Y, Long M, Li B, Deng W, Jin L, Zhao S, Wu D, He Y, Li C, Liu S, Huang Y, Zhang H, Zou L (2018) Metagenomic analysis of bacteria, fungi,bacteriophages, and helminths in the gut of giant pandas. Front Microbiol 69:1717

  • Siggers R, Siggers JM, Thymann T, Molbak L, Leser T, Jensen B et al (2008) Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138:1437–1444

    Article  PubMed  CAS  Google Scholar 

  • Simpson HL, Campbell BJ (2015) Review article: dietary fibre-microbiome interactions. Aliment Pharmacol Ther 42:158–179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stefanie H, Dowd SE, Garcia-Mazcorro JF, Steiner JRM, Suchodolski JS (2011) Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol 76:301–310

    Article  CAS  Google Scholar 

  • Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiome and host metabolism. Nature 71:242–249

    Article  CAS  Google Scholar 

  • Tun HM, Mauroo NF, Yuen CS, Ho JC, Wong MT, Leung FC (2014) Microbial diversity and evidence of novel homoacetogens in the gut of both geriatric and adult giant pandas (Ailuropoda melanoleuca). PLoS One 9:e79902

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Soest PJ, Mcqueen RW (1973) The chemistry and estimation of fibre. Proc Nutr Soc 32:123–130

    Article  PubMed  Google Scholar 

  • Wang H, Zhong H, Hou R, Ayala J, Liu G, Yuan S et al (2017) A diet diverse in bamboo parts is important for Giant panda ( Ailuropoda melanoleuca ) metabolism and health. Sci Rep 7:3377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wei F, Wang X, Wu Q (2015) The giant panda gut microbiome. Trends Microbiol 23:450–452

    Article  PubMed  CAS  Google Scholar 

  • Williams CL, Willard S, Kouba A, Sparks D, Holmes W, Falcone J, Williams CH, Brown A (2013) Dietary shifts affect the gastrointestinal microflora of the giant panda (Ailuropoda melanoleuca). J Ani Physiol Ani Nutri 97:577–585

  • Wu Q, Wang X, Ding Y, Hu Y, Nie Y, Wei W et al (2017) Seasonal variation in nutrient utilization shapes gut microbiome structure and function in wild giant pandas. Proceedings Biological Sciences 284:20170955

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xue Z, Zhang W, Wang L, Hou R, Zhang M, Fei L et al (2015) The bamboo-eating Giant panda harbors a carnivore-like gut microbiome, with excessive seasonal variations. mBio6:00022–00015

    Google Scholar 

  • Zhang W, Liu W, Hou R, Zhang L, Schmitz-Esser S, Sun H et al (2018). Age-associated microbiome shows the giant panda lives on hemicelluloses, not on cellulose. ISME J 12:1319–1328

  • Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T et al (2016) Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352:565

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou YK, Shen XY, Hou CL (2017) Diversity and antimicrobial activity of culturable fungi from fishscale bamboo ( Phyllostachys heteroclada ) in China. World Journal of Microbiology & Biotechnology 33:104

    Article  CAS  Google Scholar 

  • 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 microbiome is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6:1415–1426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Open Project of  SFGA  on Conservation Biology of Rare Animals in the Giant Panda National Park (CCRCGP, No. KLSFGAGP2020.003), Scientific Backbone Research Project (10912-2019KYGG201530) and Postdoctoral Science Foundation of Chengdu University of Technology.

Author information

Author notes

  1. Lei Jin, Daifu Wu and Caiwu Li contributed equally to this work.

Authors and Affiliations

  1. Department of Applied Microbiology, College of Resources, Sichuan Agricultural University, Chengdu, China

    Lei Jin, Shengzhi Yang, Bei Li & Likou Zou

  2. Key Laboratory of State Forestry and Grassland Administration (SFGA) on Conservation Biology of Rare Animals in the Giant Panda National Park, the China Conservation and Research Center for the Giant Panda (CCRCGP), Dujiangyan, China

    Daifu Wu, Caiwu Li, Yaowu Xiong, Rongping Wei, Guiquan Zhang, Wenwen Deng, Ti Li, Zhizhong Zhang, Yan Huang, Hemin Zhang & Yongguo He

  3. Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China

    Anyun Zhang

  4. College of Tourism, and Town and Country Planning, Chengdu University of Technology, Chengdu, China

    Xin Pan

Authors
  1. Lei Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daifu Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caiwu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anyun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaowu Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rongping Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guiquan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shengzhi Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wenwen Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ti Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Bei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Xin Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Zhizhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Hemin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Yongguo He
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Likou Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hemin Zhang, Yongguo He or Likou Zou.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 632 kb)

ESM 2

(DOCX 57 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jin, L., Wu, D., Li, C. et al. Bamboo nutrients and microbiome affect gut microbiome of giant panda. Symbiosis 80, 293–304 (2020). https://doi.org/10.1007/s13199-020-00673-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-020-00673-0

Keywords

Search

Navigation