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The impact of anthelmintic treatment on gut bacterial and fungal communities in diagnosed parasite-free sika deer Cervus nippon

  • Applied genetics and molecular biotechnology
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Abstract

The gut microbiota, including both bacterial and fungal communities, plays vital roles in the gut homeostasis of animals, and antibiotics can lead to disorders of these microbial communities. The use of anthelmintic treatment to control parasitic infection has long been a standard practice, although its impact on the gut microbiota of healthy sika deer is relatively unknown. This study used next-generation sequencing based on 16S/18S/ITS rRNA genes to investigate the shifts in fecal bacterial and fungal communities in parasite-free sika deer after treatment with fenbendazole and ivermectin tablets. The α-diversity of both bacterial and fungal communities was significantly decreased (P < 0.05) after treatment, as were the bacterial genus Bacteroides and fungal genus Candida (P < 0.05). The results of β-diversity, LEfSe analysis, core community’s analysis, taxonomic composition, and functional prediction of fungal and bacterial communities confirmed the substantial impacts of anthelmintic treatment on the function and structure of the intestinal microbiota of sika deer. Nevertheless, many lines of evidence, including β-diversity, LEfSe analysis and functional prediction analysis, suggested that the anthelmintics exerted more significant influences on fungal communities than on bacterial communities, suggesting that more attention should be paid to the changes in fungal communities of sika deer under anthelmintic treatment. The present study provides evidence to support the assumption that anthelmintic drugs modify the gut microbiota of deer and serves as the first trial to test the potential effects of anthelmintics on mycobiota in ruminants using high-throughput sequencing techniques.

Key Points

• Anthelmintic treatment showed significant effects on the gut microbiota of sika deer.

• Fungi were more strongly affected by anthelmintic treatment than bacteria.

• The profile of mycobiota provides essential data that were previously absent.

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Data availability

The nucleotide sequence data reported are available in the GenBank databases under the accession number PRJNA615354. If requested, the database will withhold the release of data until publication.

References

  • Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AF, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol 186(2):281–285

    PubMed  Google Scholar 

  • Bi Y, Cox MS, Zhang F, Suen G, Zhang N, Tu Y, Diao Q (2019) Feeding modes shape the acquisition and structure of the initial gut microbiota in newborn lambs. Environ Microbiol 21(7):2333–2346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brook I, Frazier EH (2000) Aerobic and anaerobic microbiology in intra-abdominal infections associated with diverticulitis. J Med Microbiol 49(9):827–830

    PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho I, Yamanishi S, Cox L, Methé BA, Zavadil J, Li K, Gao Z, Mahana D, Raju K, Teitler I, Li H, Alekseyenko AV, Blaser MJ (2012) Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488(7413):621–626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. Plymouth: Plymouth Marine Laboratory

  • Costa MC, Arroyo LG, Allen-Vercoe E, Stämpfli HR, Kim PT, Sturgeon A, Weese JS (2012) Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene. PLoS One 7(7):e41484

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado ML, Singh P, Funk JA, Moore JA, Cannell EM, Kanesfsky J, Manning SD, Scribner KT (2017) Intestinal microbial community dynamics of white-tailed deer (Odocoileus virginianus) in an agroecosystem. Microb Ecol 74:496–506

    PubMed  Google Scholar 

  • Dollive S, Chen YY, Grunberg S, Bittinger K, Hoffmann C, Vandivier L, Cuff C, Lewis JD, Wu GD, Bushman FD (2013) Fungi of the murine gut: episodic variation and proliferation during antibiotic treatment. PLoS One 8(8):e71806

    CAS  PubMed  PubMed Central  Google Scholar 

  • Donaldson GP, Ladinsky MS, Yu KB, Sanders JG, Yoo BB, Chou WC, Conner ME, Earl AM, Knight R, Bjorkman PJ, Mazmanian SK (2018) Gut microbiota utilize immunoglobulin A for mucosal colonization. Science 360(6390):795–800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Easton AV, Quiñones M, Vujkovic-Cvijin I, Oliveira RG, Kepha S, Odiere MR, Anderson RM, Belkaid Y, Nutman TB (2019) The impact of anthelmintic treatment on human gut microbiota based on cross-sectional and pre-and postdeworming comparisons in western Kenya. Mbio 10(2):e00519–e00519

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elzinga SE, Weese JS, Adams AA (2016) Comparison of the fecal microbiota in horses with equine metabolic syndrome and metabolically normal controls fed a similar all-forage diet. J Equine Vet Sci 44:9–16

    Google Scholar 

  • Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, Rosenbaum M, Gordon JI (2013) The long-term stability of the human gut microbiota. Science 341(6141):1237439

    PubMed  PubMed Central  Google Scholar 

  • Fouhy F, Guinane CM, Hussey S, Wall R, Ryan CA, Dempsey EM, Murphy B, Ross RP, Fitzgerald GF, Stanton C, Cotter PD (2012) High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother 56(11):5811–5820

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fung TC, Olson CA, Hsiao EY (2017) Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 20:145–155

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guan Y, Yang H, Han S, Feng L, Wang T, Ge J (2018) Comparison of the gut microbiota composition between wild and captive sika deer (Cervus nippon hortulorum) from feces by high-throughput sequencing. AMB Express 7(1):212

    Google Scholar 

  • Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, 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(2):301–310

    CAS  PubMed  Google Scholar 

  • He F, Zhai J, Zhang L, Liu D, Ma Y, Rong K, Xu Y, Ma J (2018) Variations in gut microbiota and fecal metabolic phenotype associated with Fenbendazole and Ivermectin Tablets by 16S rRNA gene sequencing and LC/MS-based metabolomics in Amur tiger. Biochem Biophys Res Commun 499(3):447–453

    CAS  PubMed  Google Scholar 

  • Hu XL, Liu G, Li YM, Wei YT, Lin SB, Liu SQ, Zheng YL, Hu DF (2018) High-throughput analysis reveals seasonal variation of the gut microbiota composition within forest musk deer (Moschus berezovskii). Front Microbiol 9:1674

  • Hu XL, Liu G, Wang WX, Zhou R, Liu SQ, Li LH, Hu DF (2016) Methods of preservation and flotation for the detection of nematode eggs and coccidian oocysts in faeces of the forest musk deer. J Helminthol 90(6):680–684

    CAS  PubMed  Google Scholar 

  • Isaac S, Scher JU, Djukovic A, Jiménez N, Littman DR, Abramson SB, Pamer EG, Ubeda C (2016) Short-and long-term effects of oral vancomycin on the human intestinal microbiota. J Antimicrob Chemother 72(1):128–136

    PubMed  PubMed Central  Google Scholar 

  • Jagla E, Spiewak J, Zalesny G, Popiołek M (2013) Effect of storage and preservation of horse faecal samples on the detectability and viability of Strongylid nematode eggs and larvae. Bull Vet Inst Pulawy 57:161–165

    CAS  Google Scholar 

  • Jami E, Israel A, Kotser A, Mizrahi I (2013) Exploring the bovine rumen bacterial community from birth to adulthood. ISME J 7:1069–1079

    PubMed  PubMed Central  Google Scholar 

  • Kunz IG, Reed KJ, Metcalf JL, Hassel DM, Coleman RJ, Hess TM, Coleman SJ (2019) Equine fecal microbiota changes associated with anthelmintic administration. J Equine Vet Sci 77:98–106

    PubMed  Google Scholar 

  • Lange K, Buerger M, Stallmach A, Bruns T (2016) Effects of antibiotics on gut microbiota. Dig Dis 34(3):260–268

    PubMed  Google Scholar 

  • Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023

    CAS  Google Scholar 

  • Liu J, Yang J, Guan G, Liu A, Wang B, Luo J, Yin H (2016) Molecular detection and identification of piroplasms in sika deer (Cervus nippon) from Jilin Province, China. Parasit Vectors 9(1):156

    PubMed  PubMed Central  Google Scholar 

  • Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55(2):205–211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J 17(1):10–12

    Google Scholar 

  • Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453(7195):620–625

    CAS  PubMed  Google Scholar 

  • McCullough DR, Takatsuki S, Kaji K (2009) Sika deer: biology and management of native and introduced populations. Springer, Tokyo

    Google Scholar 

  • Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J Clin Invest 124(10):4212–4218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morgun A, Dzutsev A, Dong X, Greer RL, Sexton DJ, Ravel J, Schuster M, Schuster W, Matzinger P, Shulzhenko N (2015) Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks. Gut 64(11):1732–1743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Münger E, Montiel-Castro AJ, Langhans W, Pacheco-López G (2018) Reciprocal interactions between gut microbiota and host social behavior. Front Integr Neurosci 12:21

    PubMed  PubMed Central  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) Funguild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Google Scholar 

  • Odds FC, Davidson AD, Jacobsen MD, Tavanti A, Whyte J, Kibbler CC, Ellis DH, Maiden MCJ, Shaw DJ, Gow NAR (2006) Candida albicans strain maintenance, replacement, and microvariation demonstrated by multilocus sequence typing. J Clin Microbiol 44(10):3647–3658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oppliger A, Clobert J, Lecomte J, Lorenzon P, Boudjemadi K, John-Alder HB (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol Lett 1:129–138

    Google Scholar 

  • Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, Timmis KN, Schreiber S (2004) Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 53(5):685–693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peachey LE, Molena R, Jenkins T, Cesare AD, Traversa D, Hodgkinson J, Cantacessi C (2018) The relationships between faecal egg counts and gut microbial composition in UK Thoroughbreds infected by cyathostomins. Int J Parasitol 48(6):403–412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peterfreund GL, Vandivier LE, Sinha R, Marozsan AJ, Olson WC, Zhu J, Bushman FD (2012) Succession in the gut microbiome following antibiotic and antibody therapies for Clostridium difficile. PLoS One 7:e46966

    CAS  PubMed  PubMed Central  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 41:590–596

    Google Scholar 

  • Rinaldi L, Coles GC, Maurelli MP, Musella V, Cringoli G (2011) Calibration and diagnostic accuracy of simple floatation, McMaster and FLOTAC for parasite egg counts in sheep. Vet Parasitol 177:345–352

    CAS  PubMed  Google Scholar 

  • Robinson CJ, Young VB (2010) Antibiotic administration alters the community structure of the gastrointestinal microbiota. Gut Microbes 1(4):279–284

    PubMed  PubMed Central  Google Scholar 

  • Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, Tuohy K (2018) Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr 57(1):1–24

    CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert AM, Sinani H, Schloss PD (2015) Antibiotic-induced alterations of the murine gut microbiota and subsequent effects on colonization resistance against Clostridium difficile. Mbio 6:e00974

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shade A (2017) Diversity is the question, not the answer. ISME J 11:1–6

    PubMed  Google Scholar 

  • Shanks OC, Kelty CA, Archibeque S, Jenkins M, Newton RJ, McLellan SL, Huse SM, Sogin ML (2011) Community structures of fecal bacteria in cattle from different animal feeding operations. Appl Environ Microbiol 77:2992–3001

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33(9):496–503

    CAS  PubMed  Google Scholar 

  • Sommer F, Bäckhed F (2013) The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11(4):227–238

    CAS  PubMed  Google Scholar 

  • Standaert-Vitse A, Jouault T, Vandewalle P, Mille C, Seddik M, Sendid B, Mallet JM, Colombel JF, Poulain D (2006) Candida albicans is an immunogen for anti-Saccharomyces cerevisiae antibody markers of Crohn’s disease. Gastroenterology 130(6):1764–1775

    CAS  PubMed  Google Scholar 

  • Stecher B, Maier L, Hardt WD (2013) ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11:277–284

    CAS  PubMed  Google Scholar 

  • Suhr MJ, Banjara N, Hallen-Adams HE (2016) Sequence-based methods for detecting and evaluating the human gut mycobiome. Lett Appl Microbiol 62(3):209–215

    CAS  PubMed  Google Scholar 

  • Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243–246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thoetkiattikul H, Mhuantong W, Laothanachareon T, Tangphatsornruang S, Pattarajinda V, Eurwilaichitr L, Champreda V (2013) Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing. Curr Microbiol 67(2):130–137

    CAS  PubMed  Google Scholar 

  • Valdes AM, Walter J, Segal E, Spector TD (2018) Role of the gut microbiota in nutrition and health. BMJ 361:k2179

    PubMed  PubMed Central  Google Scholar 

  • Videnska P, Faldynova M, Juricova H, Babak V, Sisak F, Havlickova H, Rychlik I (2013) Chicken faecal microbiota and disturbances induced by single or repeated therapy with tetracycline and streptomycin. BMC Vet Res 9(1):30

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Ze Yang, Qinglong Yang, and other breeders of Breeding Center of sika deer in Jiangxi Province for their valuable suggestions on sample collection.

Author contribution statement

XH, WZ, and YZ conceived of the study. YX, WZ, and YZ performed research. GL and YW analyzed data. XH and DH wrote the paper. All authors read and approved the manuscript.

Funding

This work was supported by the Department of Education of Jiangxi Province (GJJ180228).

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Correspondence to Weiwei Zhang or Yunlin Zheng.

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All the experiments of this study were performed on the basis of guidelines of the Institution of Animal Care and the Ethics Committee of Jiangxi Agricultural University

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Hu, X., Xu, Y., Liu, G. et al. The impact of anthelmintic treatment on gut bacterial and fungal communities in diagnosed parasite-free sika deer Cervus nippon. Appl Microbiol Biotechnol 104, 9239–9250 (2020). https://doi.org/10.1007/s00253-020-10838-y

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