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Molecular & Cellular Toxicology

, Volume 16, Issue 1, pp 63–72 | Cite as

Impact of zinc oxide nanoparticles on the bacterial community of Hydra magnipapillata

  • Ade Yamindago
  • Nayun Lee
  • Seonock Woo
  • Seungshic YumEmail author
Original Article
  • 33 Downloads

Abstract

Backgrounds

Zinc oxide nanoparticles (ZnO NPs) are extensively used for various products. In this study, the effects of ZnO NPs exposure in diversity and community composition of the bacteria associated with H. magnipapillata were investigated. This study provides insight into possible impacts of ZnO NPs on aquatic organisms.

Methods

454-pyrosequencing analysis of the bacterial 16S rRNA gene was applied to H. magnipapillata after exposure to 10 mg/L ZnO NPs (Ø 20 nm).

Results

Acute exposure to ZnO NPs changed the diversity and compositions of the associated bacteria. The composition of Curvibacter decreased, but Flectobacillus and Delftia increased; these two genera are known to have beneficial functions.

Conclusion

The changes in diversity and composition of the associated bacteria may indicate the possible mechanisms by which the associated bacteria maintain their mutual interactions and support the health of their host after exposure to ZnO NPs.

Keywords

Hydra-associated bacteria Nanomaterial 16S rRNA gene-based metagenomic Bacterial composition 

Notes

Acknowledgements

This research was supported by a grant from Marine Biotechnology Programs (20170305), Development of Biomedical materials based on marine proteins funded by Ministry of Oceans and Fisheries, Republic of Korea and NRF-2017R1A2B2012541.

Compliance with ethical standards

Conflict of interest

Ade Yamindago, Nayun Lee, Seonock Woo and Seungshic Yum declare that they have no conflict of interest.

Supplementary material

13273_2019_58_MOESM1_ESM.xlsx (11 kb)
Table S1. Taxonomic classification and compositions of bacteria associated with H. magnipapillata at the phylum level after exposure to ZnO NPs
13273_2019_58_MOESM2_ESM.xlsx (37 kb)
Table S2. Taxonomic classification and compositions of bacteria associated with H. magnipapillata at the species level after exposure to ZnO NPs

References

  1. Altschul SF et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  2. Augustin R et al (2017) A secreted antibacterial neuropeptide shapes the microbiome of Hydra. Nat Commun 8:698PubMedPubMedCentralGoogle Scholar
  3. Baek M et al (2011) Factors influencing the cytotoxicity of zinc oxide nanoparticles: particle size and surface charge. J Phys: Conf Ser 304:012044Google Scholar
  4. Bautista-Hernández DA, Ramírez-Burgos LI, Duran-Páramo E, Fernández-Linares L (2012) Zinc and lead biosorption by Delftia tsuruhatensis: a bacterial strain resistant to metals isolated from mine tailings. J Water Resour Protect 4:207–216Google Scholar
  5. Chun J, Kim KY, Lee JH, Choi Y (2010) The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol 10:101PubMedPubMedCentralGoogle Scholar
  6. Devine SP, Pelletreau KN, Rumpho ME (2012) 16S rDNA-based metagenomic analysis of bacterial diversity associated with two populations of the kleptoplastic sea slug Elysia chlorotica and its algal prey Vaucheria litorea. Biol Bull 223:138–154PubMedGoogle Scholar
  7. Dyksma S et al (2016) Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. ISME J 10:1939–1953PubMedPubMedCentralGoogle Scholar
  8. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200PubMedPubMedCentralGoogle Scholar
  9. Fiore CL, Jarett JK, Olson ND, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 18:455–463PubMedGoogle Scholar
  10. Franzenburg S et al (2013) Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc Natl Acad Sci USA 110:E3730–E3738PubMedGoogle Scholar
  11. Fraune S, Bosch TCG (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci USA 104:13146–13151PubMedGoogle Scholar
  12. Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. Bioessays 32:571–580PubMedGoogle Scholar
  13. Fraune S, Abe Y, Bosch TCG (2009) Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota. Environ Microbiol 11:2361–2369PubMedGoogle Scholar
  14. Fraune S et al (2015) Bacteria–bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. ISME J 9:1543–1556PubMedGoogle Scholar
  15. Gihring TM et al (2011) A limited microbial consortium is responsible for extended bioreduction of uranium in a contaminated aquifer. Appl Environ Microbiol 77:5955–5965PubMedPubMedCentralGoogle Scholar
  16. Godlewski M et al (2011) Zinc oxide for electronic, photovoltaic and optoelectronic applications. Low Temp Phys 37:235–240Google Scholar
  17. Gong J et al (2016) Protist-bacteria associations: Gammaproteobacteria and Alphaproteobacteria are prevalent as digestion-resistant bacteria in ciliated protozoa. Front Microbiol 7:498PubMedPubMedCentralGoogle Scholar
  18. Grasis JA et al (2014) Species-specific viromes in the ancestral holobiont Hydra. PLoS One 9:e109952PubMedPubMedCentralGoogle Scholar
  19. Hahn MW, Moore ER, Hofle MG (1999) Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl Environ Microbiol 65:25–35PubMedPubMedCentralGoogle Scholar
  20. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27PubMedGoogle Scholar
  21. Han J et al (2005) Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Syst Appl Microbiol 28:66–76PubMedGoogle Scholar
  22. Hanna SK, Miller RJ, Muller EB, Nisbet RM, Lenihan HS (2013) Impact of engineered zinc oxide nanoparticles on the individual performance of Mytilus galloprovincialis. PLoS One 8:e61800PubMedPubMedCentralGoogle Scholar
  23. He L, Liu Y, Mustapha A, Lin M (2011) Antifungal activity of zinc oxide nanoparticles against Botrytis cinerea and Penicillium expansum. Microbiol Res 166:207–215PubMedGoogle Scholar
  24. Hoffmann F et al (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11:2228–2243PubMedGoogle Scholar
  25. Johnston CW et al (2013) Gold biomineralization by a metallophore from a gold-associated microbe. Nat Chem Biol 9:241–243PubMedGoogle Scholar
  26. Kalyuhznaya MG et al (2009) Methylophilaceae link methanol oxidation to denitrification in freshwater lake sediment as suggested by stable isotope probing and pure culture analysis. Environ Microbiol Rep 1:385–392PubMedGoogle Scholar
  27. Kim OS et al (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721PubMedGoogle Scholar
  28. Kulkarni SS, Shirsat MD (2015) Optical and structural properties of Zinc oxide nanoparticles. Int J Adv Res Phys Sci 2:14–18Google Scholar
  29. Kumar SS, Venkateswarlu P, Rao VR, Rao GN (2013) Synthesis, characterization and optical properties of zinc oxide nanoparticles. Int Nano Lett 3:30Google Scholar
  30. Liu R, Ge Y, Holden PA, Cohen Y (2015) Analysis of soil bacteria susceptibility to manufactured nanoparticles via data visualization. Beilstein J Nanotechnol 6:1635–1651PubMedPubMedCentralGoogle Scholar
  31. Liu S et al (2016) The host shapes the gut microbiota via fecal MicroRNA. Cell Host Microbe 19:32–43PubMedPubMedCentralGoogle Scholar
  32. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585PubMedPubMedCentralGoogle Scholar
  33. Magalhaes C, Bano N, Wiebe WJ, Hollibaugh JT, Bordalo AA (2007) Composition and activity of beta-Proteobacteria ammonia-oxidizing communities associated with intertidal rocky biofilms and sediments of the Douro River estuary, Portugal. J Appl Microbiol 103:1239–1250PubMedGoogle Scholar
  34. Meli K, Kamika I, Keshri J, Momba MN (2016) The impact of zinc oxide nanoparticles on the bacterial microbiome of activated sludge systems. Sci Rep 6:39176PubMedPubMedCentralGoogle Scholar
  35. Niepceron M et al (2013) Gammaproteobacteria as a potential bioindicator of a multiple contamination by polycyclic aromatic hydrocarbons (PAHs) in agricultural soils. Environ Pollut 180:199–205PubMedGoogle Scholar
  36. Pendashte H, Shariati F, Keshavarz A, Ramzanpour Z (2013) Toxicity of zinc oxide nanoparticles to Chlorella vulgaris and Scenedesmus dimorphus algae species. World J Fish Mar Sci 5:563–570Google Scholar
  37. Pietschke C et al (2017) Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts. Proc Natl Acad Sci USA 114:E8488–E8497PubMedGoogle Scholar
  38. Proenca DN et al (2010) Diversity of bacteria associated with Bursaphelenchus xylophilus and other nematodes isolated from Pinus pinaster trees with pine wilt disease. PLoS One 5:e15191PubMedPubMedCentralGoogle Scholar
  39. Schloss PD et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedPubMedCentralGoogle Scholar
  40. Scott KM, Cavanaugh CM (2007) CO2 uptake and fixation by endosymbiotic chemoautotrophs from the bivalve Solemya velum. Appl Environ Microbiol 73:1174–1179PubMedGoogle Scholar
  41. Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503PubMedPubMedCentralGoogle Scholar
  42. Song Z et al (2011) Characterization of optical properties of ZnO nanoparticles for quantitative imaging of transdermal transport. Biomed Opt Express 2:3321–3333PubMedPubMedCentralGoogle Scholar
  43. Sugiyama T, Fujisawa T (1977) Genetic analysis of developmental mechanisms in hydra I. Sexual reproduction of Hydra magnipapillata and isolation of mutants. Dev Growth Differ 19:187–200Google Scholar
  44. Supha C, Boonto Y, Jindakaraked M, Ananpattarachai J, Kajitvichyanukul P (2015) Long-term exposure of bacterial and protozoan communities to TiO2 nanoparticles in an aerobic-sequencing batch reactor. Sci Technol Adv Mater 16:034609PubMedPubMedCentralGoogle Scholar
  45. Willems A, De Ley J, Gillis M, Kersters K (1991) Comamonadaceae, a new family encompassing the Acidovorans rRNA complex, including Variovorax paradoxus gen. nov., comb. nov. for Alcaligenes paradoxus (Davis 1969). Int J Syst Bacteriol 41:445–450Google Scholar
  46. Williams K et al (2015) Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gut-associated immune responses in the ileum of Sprague-Dawley rats. Nanotoxicology 9:279–289PubMedGoogle Scholar
  47. Xie Y, He Y, Irwin PL, Jin T, Shi X (2011) Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Appl Environ Microbiol 77:2325–2331PubMedPubMedCentralGoogle Scholar
  48. Yamindago A, Lee N, Woo S, Yum S (2017) Microbiota changes in diseased Hydra magnipapillata. Toxicol Environ Health Sci 9:291–299Google Scholar
  49. Yamindago A et al (2018) Acute toxic effects of zinc oxide nanoparticles on Hydra magnipapillata. Aquat Toxicol 205:130–139PubMedGoogle Scholar
  50. Zhu X, Wang J, Zhang X, Chang Y, Chen Y (2009) The impact of ZnO nanoparticle aggregates on the embryonic development of zebrafish (Danio rerio). Nanotechnology 20:195103PubMedGoogle Scholar

Copyright information

© The Korean Society of Toxicogenomics and Toxicoproteomics and Springer Nature B.V. 2019

Authors and Affiliations

  • Ade Yamindago
    • 1
    • 2
    • 3
  • Nayun Lee
    • 1
  • Seonock Woo
    • 4
  • Seungshic Yum
    • 1
    • 2
    Email author
  1. 1.Ecological Risk Research DivisionKorea Institute of Ocean Science and Technology (KIOST)GeojeRepublic of Korea
  2. 2.Applied Ocean ScienceUniversity of Science and Technology (UST)DaejeonRepublic of Korea
  3. 3.Faculty of Fisheries and Marine ScienceBrawijaya UniversityMalangRepublic of Indonesia
  4. 4.Marine Biotechnology Research CenterKorea Institute of Ocean Science and Technology (KIOST)BusanRepublic of Korea

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