Current Microbiology

, Volume 75, Issue 10, pp 1352–1361 | Cite as

Fecal Bacteriome and Mycobiome in Bats with Diverse Diets in South China

  • Juan Li
  • Linmiao Li
  • Haiying Jiang
  • Lihong Yuan
  • Libiao Zhang
  • Jing-e Ma
  • Xiujuan Zhang
  • Minhua Cheng
  • Jinping ChenEmail author


Bats can be divided into frugivory, nectarivory, insectivory, and sanguivory based on their diets, and are therefore ideal wild animal models to study the relationship between diets and intestinal microflora. Early studies of bat gut bacteria showed that the diversity and structure of intestinal bacterial communities in bats are closely related to dietary changes. Worthy of note, intestinal microbes are composed of bacteria, fungi, protozoa, and archaea. Although the number of gut fungi is much lower than that of gut bacteria, they also play an important role in maintaining the host homeostasis. However, there are still few reports on the relationship between the gut mycobiota and the dietary habits of the host. In addition, bats have also been shown to naturally transmit pathogenic viruses and bacteria through their feces and saliva, but fungal infections from bat are less studied. Here, we used high-throughput sequencing of bacterial 16S and eukaryotic 18S rRNA genes in the V4 and V9 regions to characterize fecal bacterial and fungal microbiota in phytophagous and insectivorous bats in South China. The results show that the gut microbiota in bats were dominated by bacterial phyla Proteobacteria, Firmicutes, Tenericutes and Bacteroidetes, and fungal phyla Ascomycota and Basidiomycota. There was a significant difference in the diversity of bacterial and fungal microbiota between the groups, in addition to specific bacteria and fungi populations on each of them. Of note, the number of fungi in the feces of herbivorous bats is relatively higher. Most of these fungi are foodborne and are also pathogens of humans and other animals. Thus, bats are natural carriers of fungal pathogens. The current study expands the understanding of the bat gut bacterial and fungal mycobiota and provides further insight into the transmission of fungal pathogens.



This project was supported by the PlanningFunds of Science and Technology of Guangdong Province (2016B070701016 and 2013B031500006), the Funds for Environment Construction and Capacity Building of GDAS’ Research Platform (2016GDASPT-0107), and the GDAS Special Project of Science and Technology Development (2017GDASCX-0107).

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

284_2018_1530_MOESM1_ESM.tif (124.5 mb)
Supplementary material 1 (TIF 127518 KB)
284_2018_1530_MOESM2_ESM.tif (26.3 mb)
Supplementary material 2 (TIF 26896 KB)
284_2018_1530_MOESM3_ESM.tif (100.6 mb)
Supplementary material 3 (TIF 103046 KB)
284_2018_1530_MOESM4_ESM.tif (144.8 mb)
Supplementary material 4 (TIF 148264 KB)
284_2018_1530_MOESM5_ESM.xlsx (17 kb)
Supplementary material 5 (XLSX 17 KB)


  1. 1.
    Altringham JD, Hammond L, Mcowat T (1996) Bats: biology and behaviour. Oxford University Press, OxfordGoogle Scholar
  2. 2.
    Ancillotto L, Ariano A, Nardone V, Budinski I, Rydell J, Russo D (2017) Effects of free-ranging cattle and landscape complexity on bat foraging: implications for bat conservation and livestock management. Agric Ecosyst Environ 241:54–61. CrossRefGoogle Scholar
  3. 3.
    Arendrup MC, Boekhout T, Akova M, Meis JF, Cornely OA, Lortholary O, European Society of Clinical M, Infectious Diseases Fungal Infection Study G, European Confederation of Medical M (2014) ESCMID and ECMM joint clinical guidelines for the diagnosis and management of rare invasive yeast infections. Clin Microbiol Infect 20(Suppl 3):76–98. CrossRefPubMedGoogle Scholar
  4. 4.
    Avena CV, Parfrey LW, Leff JW, Archer HM, Frick WF, Langwig KE, Kilpatrick AM, Powers KE, Foster JT, McKenzie VJ (2016) Deconstructing the bat skin microbiome: influences of the host and the environment. Front Microbiol 7:1753. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Banskar S, Bhute SS, Suryavanshi MV, Punekar S, Shouche YS (2016) Microbiome analysis reveals the abundance of bacterial pathogens in Rousettus leschenaultii guano. Sci Rep 6:36948. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Banskar S, Mourya DT, Shouche YS (2016) Bacterial diversity indicates dietary overlap among bats of different feeding habits. Microbiol Res 182:99–108. CrossRefPubMedGoogle Scholar
  7. 7.
    Berthinussen A, Altringham J (2012) The effect of a major road on bat activity and diversity. J Appl Ecol 49(1):82–89. CrossRefGoogle Scholar
  8. 8.
    Bhadra B, Singh PK, Rao RS, Shivaji S (2008) Blastobotrys serpentis sp. nov., isolated from the intestine of a Trinket snake (Elaphe sp., Colubridae). FEMS Yeast Res 8(3):492–498. CrossRefPubMedGoogle Scholar
  9. 9.
    Botelho NS, de Paula SB, Panagio LA, Pinge-Filho P, Yamauchi LM, Yamada-Ogatta SF (2012) Candida species isolated from urban bats of Londrina-Parana, Brazil and their potential virulence. Zoonoses Public Health 59(1):16–22. CrossRefPubMedGoogle Scholar
  10. 10.
    Brilhante RS, Maia-Junior JE, Oliveira JS, Guedes GM, Silva AL, Moura FB, Sales JA, Castelo-Branco DS, Sidrim JJ, Cordeiro RA, Pereira-Neto WA, Rocha MF (2016) Yeasts from the microbiota of bats: a focus on the identification and antimicrobial susceptibility of cryptic species of Candida. J Med Microbiol 65(10):1225–1228. CrossRefPubMedGoogle Scholar
  11. 11.
    Brown BP, Wernegreen JJ (2016) Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants. BMC Microbiol 16(1):140. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    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. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Carrillo-Araujo M, Tas N, Alcantara-Hernandez RJ, Gaona O, Schondube JE, Medellin RA, Jansson JK, Falcon LI (2015) Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies. Front Microbiol 6:447. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43(4):783–791. CrossRefPubMedGoogle Scholar
  15. 15.
    Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, Collman RG, Bushman FD, Li H (2012) Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28(16):2106–2113. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Colston TJ, Jackson CR (2016) Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol 25(16):3776–3800. CrossRefPubMedGoogle Scholar
  17. 17.
    Daniel DS, Ng YK, Chua EL, Arumugam Y, Wong WL, Kumaran JV (2013) Isolation and identification of gastrointestinal microbiota from the short-nosed fruit bat Cynopterus brachyotis. Microbiol Res 168(8):485–496. CrossRefPubMedGoogle Scholar
  18. 18.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563. CrossRefPubMedGoogle Scholar
  19. 19.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Dietrich M, Kearney T, Seamark EC, Markotter W (2017) The excreted microbiota of bats: evidence of niche specialisation based on multiple body habitats. Fems Microbiol Lett. PubMedCrossRefGoogle Scholar
  21. 21.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. CrossRefPubMedGoogle Scholar
  22. 22.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Endo A, Tanizawa Y, Tanaka N, Maeno S, Kumar H, Shiwa Y, Okada S, Yoshikawa H, Dicks L, Nakagawa J, Arita M (2015) Comparative genomics of Fructobacillus spp. and Leuconostoc spp. reveals niche-specific evolution of Fructobacillus spp.. BMC Genom 16:1117. CrossRefGoogle Scholar
  24. 24.
    Finke MD (2013) Complete nutrient content of four species of feeder insects. Zoo Biol 32(1):27–36. CrossRefPubMedGoogle Scholar
  25. 25.
    Gaitanis G, Magiatis P, Hantschke M, Bassukas ID, Velegraki A (2012) The Malassezia genus in skin and systemic diseases. Clin Microbiol Rev 25(1):106–141. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Gardner AL (1976) Biology of bats of the New World family Phyllostomatidae. Texas Tech Press, LubbockGoogle Scholar
  27. 27.
    Gouba N, Drancourt M (2015) Digestive tract mycobiota: a source of infection. Med Mal Infect 45(1–2):9–16. CrossRefPubMedGoogle Scholar
  28. 28.
    Hafeez R, Akhtar N, Shoaib A, Bashir U, Haider MS, Awan ZA (2015) First report of Geotrichum candidum from Pakistan causing postharvest sour rot in loquat (Eriobotrya Japonica). J Anim Plant Sci 25(6):1737–1740Google Scholar
  29. 29.
    Hallen-Adams HE, Suhr MJ (2017) Fungi in the healthy human gastrointestinal tract. Virulence 8(3):352–358. CrossRefPubMedGoogle Scholar
  30. 30.
    Hoffmann C, Dollive S, Grunberg S, Chen J, Li H, Wu GD, Lewis JD, Bushman FD (2013) Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS ONE 8(6):e66019. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hoyt JR, Sun K, Parise KL, Lu G, Langwig KE, Jiang T, Yang S, Frick WF, Kilpatrick AM, Foster JT, Feng J (2016) Widespread bat white-nose syndrome fungus, Northeastern China. Emerg Infect Dis 22(1):140–142. CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Huffnagle GB, Noverr MC (2013) The emerging world of the fungal microbiome. Trends Microbiol 21(7):334–341. CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hussain M, Hamid MI, Ghazanfar MU, Akhtar N, Raza M (2016) First report of fruit rot of strawberry caused by Geotrichum candidum in Pakistan. Plant Dis 100(9):1948. CrossRefGoogle Scholar
  34. 34.
    Jiang H, Li J, Li L, Zhang X, Yuan L, Chen J (2017) Selective evolution of Toll-like receptors 3, 7, 8, and 9 in bats. Immunogenetics 69(4):271–285. CrossRefPubMedGoogle Scholar
  35. 35.
    Kajdácsi E, Fazekas M, Antunovics Z, Sipiczki M (2008) Antagonistic metschnikowia strains isolated from fruits. Acta Microbiol Immunol Hung 55(3):363–363. CrossRefGoogle Scholar
  36. 36.
    Keenan SW, Engel AS, Elsey RM (2013) The alligator gut microbiome and implications for archosaur symbioses. Sci Rep 3:2877. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Korine C, Sanchez F, Pinshow B (2011) Effects of ethanol on food consumption and skin temperature in the Egyptian fruit bat (Rousettus aegyptiacus). Integr Comp Biol 51(3):432–440. CrossRefPubMedGoogle Scholar
  38. 38.
    Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6(10):776–788. CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Maliničová L, Hrehová Ľ, Maxinová E, Uhrin M, Pristaš P (2017) The dynamics of mediterranean horseshoe bat (Rhinolophus euryale, Chiroptera) gut microflora during hibernation. Acta Chiropterol 19(1):211–218. CrossRefGoogle Scholar
  40. 40.
    Mascarelli PE, Keel MK, Yabsley M, Last LA, Breitschwerdt EB, Maggi RG (2014) Hemotropic mycoplasmas in little brown bats (Myotis lucifugus). Parasit Vectors 7:117. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Mercier E, Peters IR, Billen F, Battaille G, Clercx C, Day MJ, Peeters D (2013) Potential role of Alternaria and Cladosporium species in canine lymphoplasmacytic rhinitis. J Small Anim Pract 54(4):179–183. CrossRefPubMedGoogle Scholar
  42. 42.
    Millan J, Lopez-Roig M, Delicado V, Serra-Cobo J, Esperon F (2015) Widespread infection with hemotropic mycoplasmas in bats in Spain, including a hemoplasma closely related to “Candidatus Mycoplasma hemohominis”. Comp Immunol Microbiol Infect Dis 39:9–12. CrossRefPubMedGoogle Scholar
  43. 43.
    Morrow JL, Frommer M, Shearman DC, Riegler M (2015) The microbiome of field-caught and laboratory-adapted Australian Tephritid fruit fly species with different host plant use and specialisation. Microb Ecol 70(2):498–508. CrossRefPubMedGoogle Scholar
  44. 44.
    Muhldorfer K (2013) Bats and bacterial pathogens: a review. Zoonoses Public Health 60(1):93–103. CrossRefPubMedGoogle Scholar
  45. 45.
    Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, Stewart CJ, Metcalf GA, Muzny DM, Gibbs RA, Ajami NJ, Petrosino JF (2017) The gut mycobiome of the human microbiome project healthy cohort. Microbiome 5(1):153. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Okmen B, Collemare J, Griffiths S, van der Burgt A, Cox R, de Wit PJ (2014) Functional analysis of the conserved transcriptional regulator CfWor1 in Cladosporium fulvum reveals diverse roles in the virulence of plant pathogenic fungi. Mol Microbiol 92(1):10–27. CrossRefPubMedGoogle Scholar
  47. 47.
    Orbach DN, Veselka N, Dzal Y, Lazure L, Fenton MB (2010) Drinking and flying: does alcohol consumption affect the flight and echolocation performance of phyllostomid bats? PLoS ONE 5(2):e8993. CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Pauli BP, Zollner PA, Haulton GS, Shao G, Shao G (2015) The simulated effects of timber harvest on suitable habitat for Indiana and northern long-eared bats. Ecosphere. CrossRefGoogle Scholar
  49. 49.
    Phillips CD, Phelan G, Dowd SE, McDonough MM, Ferguson AW, Delton Hanson J, Siles L, Ordonez-Garza N, San Francisco M, Baker RJ (2012) Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol Ecol 21(11):2617–2627. CrossRefPubMedGoogle Scholar
  50. 50.
    Pottier I, Gente S, Vernoux JP, Gueguen M (2008) Safety assessment of dairy microorganisms: Geotrichum candidum. Int J Food Microbiol 126(3):327–332. CrossRefPubMedGoogle Scholar
  51. 51.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(Database Issue):D590–D596. CrossRefGoogle Scholar
  52. 52.
    Roggenbuck M, Baerholm Schnell I, Blom N, Baelum J, Bertelsen MF, Sicheritz-Ponten T, Sorensen SJ, Gilbert MT, Graves GR, Hansen LH (2014) The microbiome of new world vultures. Nat Commun 5:5498. CrossRefPubMedGoogle Scholar
  53. 53.
    Sam QH, Chang MW, Chai LY (2017) The fungal mycobiome and its interaction with gut bacteria in the host. Int J Mol Sci. PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Sasaki Y, Ishikawa J, Yamashita A, Oshima K, Kenri T, Furuya K, Yoshino C, Horino A, Shiba T, Sasaki T, Hattori M (2002) The complete genomic sequence of Mycoplasma penetrans, an intracellular bacterial pathogen in humans. Nucleic Acids Res 30(23):5293–5300. CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Sommer F, Stahlman M, Ilkayeva O, Arnemo JM, Kindberg J, Josefsson J, Newgard CB, Frobert O, Backhed F (2016) The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep 14(7):1655–1661. CrossRefPubMedGoogle Scholar
  56. 56.
    Sonnenburg JL, Backhed F (2016) Diet-microbiota interactions as moderators of human metabolism. Nature 535(7610):56–64. CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Spencer DM, Spencer JFT, Defigueroa L, Heluane H (1992) Yeasts associated with rotting citrus-fruits in tucuman, Argentina. Mycol Res 96:891–892CrossRefGoogle Scholar
  58. 58.
    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. CrossRefPubMedGoogle Scholar
  59. 59.
    Tra Bi CY, N’Guessan FK, Kouakou CA, Jacques N, Casaregola S, Dje MK (2016) Identification of yeasts isolated from raffia wine (Raphia hookeri) produced in Cote d’Ivoire and genotyping of Saccharomyces cerevisiae strains by PCR inter-delta. World J Microbiol Biotechnol 32(8):125. CrossRefPubMedGoogle Scholar
  60. 60.
    Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242–249. CrossRefPubMedGoogle Scholar
  61. 61.
    Underhill DM, Lliev LD (2014) The mycobiota: interactions between commensal fungi and the host immune system. Nature Rev Immunol 14(6):405–416. CrossRefGoogle Scholar
  62. 62.
    Veikkolainen V, Vesterinen EJ, Lilley TM, Pulliainen AT (2014) Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerg Infect Dis 20(6):960–967. CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5(4):e1000352. CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108. CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Wu Z, Yang L, Ren X, He G, Zhang J, Yang J, Qian Z, Dong J, Sun L, Zhu Y, Du J, Yang F, Zhang S, Jin Q (2016) Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J 10(3):609–620. CrossRefPubMedGoogle Scholar
  66. 66.
    Yan L, Yang C, Tang J (2013) Disruption of the intestinal mucosal barrier in Candida albicans infections. Microbiol Res 168(7):389–395. CrossRefPubMedGoogle Scholar
  67. 67.
    Zeller S, Lempert S, Goebeler M, Hamm H, Kolb-Maurer A (2015) Cladosporium cladosporioides: a so far unidentified cause of white piedra. Mycoses 58(5):315–317. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Juan Li
    • 1
    • 2
    • 3
  • Linmiao Li
    • 3
  • Haiying Jiang
    • 1
    • 2
    • 3
  • Lihong Yuan
    • 3
  • Libiao Zhang
    • 3
  • Jing-e Ma
    • 3
  • Xiujuan Zhang
    • 3
  • Minhua Cheng
    • 4
  • Jinping Chen
    • 3
    Email author
  1. 1.Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical GardenChinese Academy of ScienceGuangzhouChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and UtilizationGuangdong Institute of Applied Biological ResourcesGuangzhouChina
  4. 4.Wuhan Chopper Biology Co., LtdWuhanChina

Personalised recommendations