Journal of Ecology and Environment

한국생태학회 (The Ecological Society of Korea)
권호 표지
DOI QR코드

DOI QR Code

Bacterial communities in the feces of insectivorous bats in South Korea

  • Injung An (Ecological Technology Research Team, National Institution of Ecology) ;
  • Byeori Kim (Ecological Technology Research Team, National Institution of Ecology) ;
  • Sungbae Joo (Ecological Observation Team, National Institution of Ecology) ;
  • Kihyun Kim (Ecological Restoration Team, National Institution of Ecology) ;
  • Taek-Woo Lee (Ecological Technology Research Team, National Institution of Ecology)
  • 투고 : 2023.10.10
  • 심사 : 2024.01.26
  • 발행 : 2024.06.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Bats serve as vectors and natural reservoir hosts for various infectious viruses, bacteria, and fungi. These pathogens have also been detected in bat feces and can cause severe illnesses in hosts, other animals, and humans. Because pathogens can easily spread into the environment through bat feces, determining the bacterial communities in bat guano is crucial to mitigate potential disease transmission and outbreaks. This study primarily aimed to examine bacterial communities in the feces of insectivorous bats living in South Korea. Fecal samples were collected after capturing 84 individuals of four different bat species in two regions of South Korea, and the bacterial microbiota was assessed through next generation sequencing of the 16S rRNA gene. The results revealed that, with respect to the relative abundance at the phylum level, Myotis bombinus was dominated by Firmicutes (47.24%) and Proteobacteria (42.66%) whereas Miniopterus fuliginosus (82.78%), Rhinolophus ferrumequinum (63.46%), and Myotis macrodactylus (78.04%) were dominated by Proteobacteria. Alpha diversity analysis showed no difference in abundance between species and a significant difference (p < 0.05) between M. bombinus and M. fuliginosus. Beta-diversity analysis revealed that Clostridium, Asaia, and Enterobacteriaceae_g were clustered as major factors at the genus level using principal component analysis. Additionally, linear discriminant analysis effect size was conducted based on relative expression information to select bacterial markers for each bat species. Clostridium was relatively abundant in M. bombinus, whereas Mycoplasma_g10 was relatively abundant in R. ferrumequinum. Our results provide an overview of bat guano microbiota diversity and the significance of pathogenic taxa for humans and the environment, highlighting a better understanding of preventing emerging diseases. We anticipate that this research will yield bioinformatic data to advance our knowledge of overall microbial genetic diversity and clustering characteristics in insectivorous bat feces in South Korea.

키워드

과제정보

This research was funded by research projects of the National Institute of Ecology, Republic of Korea, grant numbers NIE-2023-38.

참고문헌

  1. Abdelfattah A, Malacrino A, Wisniewski M, Cacciola SO, Schena L. Metabarcoding: a powerful tool to investigate microbial communities and shape future plant protection strategies. Biological Control. 2018;120:1-10. https://doi.org/10.1016/j.biocontrol.2017.07.009
  2. Brook CE, Dobson AP. Bats as 'special' reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015;23(3):172-80. https://doi.org/10.1016/j.tim.2014.12.004
  3. Dietrich M, Kearney T, Seamark ECJ, Paweska JT, Markotter W. Synchronized shift of oral, faecal and urinary microbiotas in bats and natural infection dynamics during seasonal reproduction. R Soc Open Sci. 2018;5(5):180041. https://doi.org/10.1098/rsos.180041
  4. Dietrich M, Markotter W. Studying the microbiota of bats: accuracy of direct and indirect samplings. Ecol Evol. 2019;9(4):1730-5. https://doi.org/10.1002/ece3.4842
  5. Dimkic I, Fira D, Janakiev T, Kabic J, Stupar M, Nenadic M, et al. The microbiome of bat guano: for what is this knowledge important? Appl Microbiol Biotechnol. 2021;105(4):1407-19. https://doi.org/10.1007/s00253-021-11143-y
  6. Elie C, Perret M, Hage H, Sentausa E, Hesketh A, Louis K, et al. Comparison of DNA extraction methods for 16S rRNA gene sequencing in the analysis of the human gut microbiome. Sci Rep. 2023;13(1):10279. https://doi.org/10.1038/s41598-023-33959-6
  7. Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome. 2014;2(1):6. https://doi.org/10.1186/2049-2618-2-6
  8. Gerbacova K, Malinicova L, Kiskova J, Maslisova V, Uhrin M, Pristas P. The faecal microbiome of building-dwelling insectivorous bats (Myotis myotis and Rhinolophus hipposideros) also contains antibiotic-resistant bacterial representatives. Curr Microbiol. 2020;77(9):2333-44. https://doi.org/10.1007/s00284-020-02095-z
  9. Gevers D, Knight R, Petrosino JF, Huang K, McGuire AL, Birren BW, et al. The human microbiome project: a community resource for the healthy human microbiome. PLoS Biol. 2012;10(8):e1001377. https://doi.org/10.1371/journal.pbio.1001377
  10. Gonella E, Crotti E, Rizzi A, Mandrioli M, Favia G, Daffonchio D, et al. Horizontal transmission of the symbiotic bacterium Asaia sp. In the leafhopper Scaphoideus titanus ball (Hemiptera: Cicadellidae). BMC Microbiol. 2012;12(Suppl 1):S4. https://doi.org/10.1186/1471-2180-12-S1-S4
  11. Gong L, Liu B, Wu H, Feng J, Jiang T. Seasonal dietary shifts alter the gut microbiota of avivorous bats: implication for adaptation to energy harvest and nutritional utilization. mSphere. 2021;6(4):e0046721. https://doi.org/10.1128/msphere.00467-21
  12. Hahn MW, Koll U, Schmidt J. Isolation and cultivation of bacteria. In: Hurst CJ, editor. The structure and function of aquatic microbial communities. New York: Springer; 2019. p. 313-51.
  13. Hayes JP, Loeb SC. The influences of forest management on bats in North America. In: Lacki MJ, Hayes JP, Kurta A, editors. Bats in forests: conservation and management. Baltimore: The Johns Hopkins University Press; 2007. p. 207-36.
  14. Huang Y, Sun Y, Huang Q, Lv X, Pu J, Zhu W, et al. The threat of potentially pathogenic bacteria in the feces of bats. Microbiol Spectr. 2022;10(6):e0180222. https://doi.org/10.1128/spectrum.01802-22
  15. Ingala MR, Simmons NB, Perkins SL. Bats are an untapped system for understanding microbiome evolution in mammals. mSphere. 2018;3(5):e00397-18. https://doi.org/10.1128/msphere.00397-18
  16. Kasso M, Balakrishnan M. Ecological and economic importance of bats (Order Chiroptera). Isrn Biodiversity. 2013;2013:1-9. https://doi.org/10.1155/2013/187415
  17. Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, et al. Best practices for analysing microbiomes. Nat Rev Microbiol. 2018;16(7):410-22. https://doi.org/10.1038/s41579-018-0029-9
  18. Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH. Ecosystem services provided by bats. Ann N Y Acad Sci. 2011;1223:1-38. https://doi.org/10.1111/j.1749-6632.2011.06004.x
  19. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320(5883):1647-51. https://doi.org/10.1126/science.1155725
  20. Lutz HL, Jackson EW, Webala PW, Babyesiza WS, Kerbis Peterhans JC, Demos TC, et al. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. mSystems. 2019;4(6):e00511-19. https://doi.org/10.1128/msystems.00511-19
  21. Mitchell-Jones AJ, McLeish AP. Bat workers' manual. 3rd ed. Addle-stone: Joint Nature Conservation Committee; 2004.
  22. O'Shea TJ, Cryan PM, Cunningham AA, Fooks AR, Hayman DT, Luis AD, et al. Bat flight and zoonotic viruses. Emerg Infect Dis. 2014;20(5):741-5. https://doi.org/10.3201/eid2005.130539
  23. Phillips CD, Phelan G, Dowd SE, McDonough MM, Ferguson AW, Delton Hanson J, et al. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol Ecol. 2012;21(11):2617-27. https://doi.org/10.1111/j.1365-294X.2012.05568.x
  24. Rami A, Raz A, Zakeri S, Dinparast Djadid N. Isolation and identification of Asaia sp. In Anopheles spp. Mosquitoes collected from Iranian malaria settings: steps toward applying paratransgenic tools against malaria. Parasit Vectors. 2018;11(1):367. https://doi.org/10.1186/s13071-018-2955-9
  25. Ramirez-Francel LA, Garcia-Herrera LV, Losada-Prado S, Reinoso-Florez G, Sanchez-Hernandez A, Estrada-Villegas S, et al. Bats and their vital ecosystem services: a global review. Integr Zool. 2022;17(1):2-23. https://doi.org/10.1111/1749-4877.12552
  26. Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. Biomed Res Int. 2017;2017:9351507. https://doi.org/10.1155/2017/9351507
  27. Rodriguez C, Taminiau B, Van Broeck J, Delmee M, Daube G. Clostridium difficile in food and animals: a comprehensive review. Adv Exp Med Biol. 2016;932:65-92. https://doi.org/10.1007/5584_2016_27
  28. Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, Katariya V, et al. The status of the world's land and marine mammals: diversity, threat, and knowledge. Science. 2008;322(5899):225-30. https://doi.org/10.1126/science.1165115
  29. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. https://doi.org/10.1186/gb-2011-12-6-r60
  30. Siemers BM, Schnitzler HU. Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature. 2004;429(6992):657-61. https://doi.org/10.1038/nature02547
  31. Simmons NB, Cirranello AL. Bat species of the world: a taxonomic and geographic database. Version 1.4. 2023. https://doi.org/10.5281/zenodo.8136157. Accessed 11 Jul 2023.
  32. Song SJ, Sanders JG, Delsuc F, Metcalf J, Amato K, Taylor MW, et al. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio. 2020;11(1):e02901-19. https://doi.org/10.1128/mBio.02901-19
  33. Sun DL, Gao YZ, Ge XY, Shi ZL, Zhou NY. Special features of bat microbiota differ from those of terrestrial mammals. Front Microbiol. 2020;11:1040. https://doi.org/10.3389/fmicb.2020.01040
  34. Veikkolainen V, Vesterinen EJ, Lilley TM, Pulliainen AT. Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerg Infect Dis. 2014;20(6):960-7. https://doi.org/10.3201/eid2006.130956
  35. Vengust M, Knapic T, Weese JS. The fecal bacterial microbiota of bats; Slovenia. PLoS One. 2018;13(5):e0196728. https://doi.org/10.1371/journal.pone.0196728
  36. Wilke ABB, Marrelli MT. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit Vectors. 2015;8:342. https://doi.org/10.1186/s13071-015-0959-2
  37. Wilson DE, Mittermeier RA. Handbook of the mammals of the world. Vol. 9, Bats. Barcelona: Lynx Nature Books; 2019.
  38. Wolkers-Rooijackers JCM, Rebmann K, Bosch T, Hazeleger WC. Fecal bacterial communities in insectivorous bats from the Netherlands and their role as a possible vector for foodborne diseases. Acta Chiropterologica. 2019;20(2):475-83. https://doi.org/10.3161/15081109ACC2018.20.2.017
  39. Xia Y, Sun J. Hypothesis testing and statistical analysis of microbiome. Genes Dis. 2017;4(3):138-48. https://doi.org/10.1016/j.gendis.2017.06.001
  40. Xiao G, Liu S, Xiao Y, Zhu Y, Zhao H, Li A, et al. Seasonal changes in gut microbiota diversity and composition in the greater horseshoe bat. Front Microbiol. 2019;10:2247. https://doi.org/10.3389/fmicb.2019.02247
  41. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67(5):1613-7. https://doi.org/10.1099/ijsem.0.001755
  42. Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2010;4(2):232-41. https://doi.org/10.1038/ismej.2009.112
  43. Zou W, Liang H, Wu P, Luo B, Zhou D, Liu W, et al. Correlated evolution of wing morphology and echolocation calls in bats. Front Ecol Evol. 2022;10:1031548. https://doi.org/10.3389/fevo.2022.1031548