Skip to main content
SpringerLink
Log in

Impact of Zero-Valent Iron on Freshwater Bacterioplankton Metabolism as Predicted from 16S rRNA Gene Sequence Libraries

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The application of zero-valent iron particles (ZVI) for the treatment of heavily polluted environment and its biological effects have been studied for at least two decades. Still, information on the impact on bacterial metabolic pathways is lacking. This study describes the effect of microscale and nanoscale ZVI (mZVI and nZVI) on the abundance of different metabolic pathways in freshwater bacterial communities. The metabolic pathways were inferred from metabolism modelling based on 16S rRNA gene sequence data using paprica pipeline. The nZVI changed the abundance of numerous metabolic pathways compared to a less influencing mZVI. We identified the 50 most affected pathways, where 31 were related to degradation, 17 to biosynthesis, and 2 to detoxification. The linkage between pathways was two times higher in nZVI samples compared to mZVI, and was specifically higher considering the arsenate detoxification II pathway. Limnohabitans and Roseiflexus were linked to the same pathways in both nZVI and mZVI. The prediction of metabolic pathways increases our knowledge of the impacts of nZVI and mZVI on freshwater bacterioplankton.

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

Similar content being viewed by others

References

  1. Burdușel AC, Gherasim O, Grumezescu AM et al (2018) Biomedical applications of silver nanoparticles: an up-to-date overview. Nanomaterials 8:1–25. https://doi.org/10.3390/nano8090681

    Article  CAS  Google Scholar 

  2. Bardos P, Bone B, Černík M et al (2015) Nanoremediation and international environmental restoration markets. Remediat J 26:101–108. https://doi.org/10.1002/rem

    Article  Google Scholar 

  3. Cundy AB, Hopkinson L, Whitby RLD (2008) Use of iron-based technologies in contaminated land and groundwater remediation: a review. Sci Total Environ 400:42–51. https://doi.org/10.1016/j.scitotenv.2008.07.002

    Article  CAS  PubMed  Google Scholar 

  4. Grieger KD, Fjordbøge A, Hartmann NB et al (2010) Environmental benefits and risks of zero-valent iron nanoparticles ( nZVI ) for in situ remediation: risk mitigation or trade-off ? J Contam Hydrol 118:165–183. https://doi.org/10.1016/j.jconhyd.2010.07.011

    Article  CAS  PubMed  Google Scholar 

  5. Albergaria JT, Nouws HPA, Delerue-Matos CM (2013) Ecotoxicity of nanoscale zero-valent iron particles—a review. Vigilância Sanitária em Debate 1:38–42. https://doi.org/10.3395/vd.v1i4.62en

    Article  Google Scholar 

  6. Zhang W (2003) Nanoscale iron particles for environmental remediation: an overview. J Nanoparticle Res 5:323–332. https://doi.org/10.1023/A:1025520116015

    Article  CAS  Google Scholar 

  7. Klimkova S, Cernik M, Lacinova L et al (2011) Zero-valent iron nanoparticles in treatment of acid mine water from in situ uranium leaching. Chemosphere 82:1178–1184. https://doi.org/10.1016/j.chemosphere.2010.11.075

    Article  CAS  PubMed  Google Scholar 

  8. Vogel M, Nijenhuis I, Lloyd J et al (2018) Combined chemical and microbiological degradation of tetrachloroethene during the application of Carbo-Iron at a contaminated field site. Sci Total Environ 628–629:1027–1036. https://doi.org/10.1016/j.scitotenv.2018.01.310

    Article  CAS  PubMed  Google Scholar 

  9. Czinnerová M, Vološčuková O, Marková K et al (2020) Combining nanoscale zero-valent iron with electrokinetic treatment for remediation of chlorinated ethenes and promoting biodegradation: a long-term field study. Water Res 175:115692. https://doi.org/10.1016/j.watres.2020.115692

    Article  CAS  PubMed  Google Scholar 

  10. Mueller NC, Braun J, Bruns J et al (2012) Application of nanoscale zero valent iron (NZVI) for groundwater remediation in Europe. Environ Sci Pollut Res 19:550–558. https://doi.org/10.1007/s11356-011-0576-3

    Article  CAS  Google Scholar 

  11. Nguyen NHA, Špánek R, Kasalický V et al (2018) Different effects of nano-scale and micro-scale zero-valent iron particles on planktonic microorganisms from natural reservoir water. Environ Sci Nano 5:1117–1129. https://doi.org/10.1039/C7EN01120B

    Article  CAS  Google Scholar 

  12. Němeček J, Lhotský O, Cajthaml T (2014) Nanoscale zero-valent iron application for in situ reduction of hexavalent chromium and its effects on indigenous microorganism populations. Sci Total Environ 485–486:739–747. https://doi.org/10.1016/j.scitotenv.2013.11.105

    Article  CAS  PubMed  Google Scholar 

  13. Barnes RJ, van der Gast CJ, Riba O et al (2010) The impact of zero-valent iron nanoparticles on a river water bacterial community. J Hazard Mater 184:73–80. https://doi.org/10.1016/j.jhazmat.2010.08.006

    Article  CAS  PubMed  Google Scholar 

  14. Louca S, Jacques SMS, Pires APF et al (2017) Functional structure of the bromeliad tank microbiome is strongly shaped by local geochemical conditions. Environ Microbiol 19:3132–3151. https://doi.org/10.1111/1462-2920.13788

    Article  CAS  PubMed  Google Scholar 

  15. Martinez Arbizu (2020) P. pairwise.Adonis: Pairwise multilevel comparison using adonis. R package version 0.4 Available online: https://github.com/pmartinezarbizu/pairwiseAdonis

  16. Langille MGI, Zaneveld J, Caporaso JG et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Douglas GM, Maffei VJ, Zaneveld J et al (2019) PICRUSt2: an improved and extensible approach for metagenome inference. BioRxiv 15:1–42. https://doi.org/10.1101/672295

    Article  Google Scholar 

  18. Fajardo C, García-Cantalejo J, Botías P et al (2019) New insights into the impact of nZVI on soil microbial biodiversity and functionality. J Environ Sci Heal Part A 54:157–167. https://doi.org/10.1080/10934529.2018.1535159

    Article  CAS  Google Scholar 

  19. Bowman JS, Ducklow HW (2015) Microbial communities can be described by metabolic structure: a general framework and application to a seasonally variable, depth-stratified microbial community from the coastal west antarctic peninsula. PLoS ONE 10:e0135868. https://doi.org/10.1371/journal.pone.0135868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ribas D, Cernik M, Martí V, Benito JA (2016) Improvements in nanoscale zero-valent iron production by milling through the addition of alumina. J Nanoparticle Res 18:181–192. https://doi.org/10.1007/s11051-016-3490-2

    Article  CAS  Google Scholar 

  21. Matsen FA, Kodner RB, Armbrust EV (2010) Pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform 11:538. https://doi.org/10.1186/1471-2105-11-538

    Article  Google Scholar 

  22. Karp PD, Paley SM, Krummenacker M et al (2010) Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology. Brief Bioinform 11:40–79. https://doi.org/10.1093/bib/bbp043

    Article  CAS  PubMed  Google Scholar 

  23. Oksanen AJ, Blanchet FG, Friendly M, et al (2016) Package ‘ vegan .’ https://cran.r-project.org, https://github.com/vegandevs/vegan 2.4–1:1–41

  24. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Barret Schloerke GGally v1.4.0. https://www.rdocumentation.org/packages/GGally

  26. Ševců A, El-Temsah YS, Joner EJ, Černík M (2011) Oxidative stress induced in microorganisms by zero-valent iron nanoparticles. Microbes Environ 26:271–281. https://doi.org/10.1264/jsme2.ME11126

    Article  PubMed  Google Scholar 

  27. Cerchiaro G, Coichev N (2009) Oxidative DNA damage induced by S(IV) in the presence of Cu(II) and Cu(I) complexes. J Brazilian Chem Soc 20:1302–1312

    Article  Google Scholar 

  28. Maki H, Sekiguchi M (1992) MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. J Nat 355:273–275. https://doi.org/10.1038/355273a0

    Article  CAS  Google Scholar 

  29. Patel PC, Goulhen F, Boothman C et al (2007) Arsenate detoxi W cation in a Pseudomonad hypertolerant to arsenic. Arch Microbiol 187:171–183. https://doi.org/10.1007/s00203-006-0182-9

    Article  CAS  PubMed  Google Scholar 

  30. Mateos LM, Ordóñez E, Letek M, Gil JA (2006) Corynebacterium glutamicum as a model bacterium for the bioremediation of arsenic. Int Microbiol 9:207–215

    CAS  PubMed  Google Scholar 

  31. Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92. https://doi.org/10.1016/S0014-5793(02)03186-1

    Article  CAS  PubMed  Google Scholar 

  32. Park H, Kanel SR, Choi H (2009) Arsenic removal by nano-scale zero valent iron and how it is affected by natural organic matter. ACS Symp Ser 1027:135–161. https://doi.org/10.1021/bk-2009-1027.ch008

    Article  CAS  Google Scholar 

  33. Mosaferi M, Nemati S, Khataee A et al (2014) Removal of Arsenic (III, V) from aqueous solution by nanoscale zero-valent iron stabilized with starch and carboxymethyl cellulose. J Environ Heal Sci Eng 12:74. https://doi.org/10.1186/2052-336X-12-74

    Article  Google Scholar 

  34. Chirino B, Strahsburger E, Agulló L et al (2013) Genomic and functional analyses of the 2-aminophenol catabolic pathway and partial conversion of its substrate into picolinic acid in Burkholderia xenovorans LB400. PLoS ONE 8:e75746. https://doi.org/10.1371/journal.pone.0075746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Takenaka S, Murakami S, Shinke R, Aoki K (1998) Metabolism of 2-aminophenol by Pseudomonas sp. AP-3: modified meta-cleavage pathway. Arch Microbiol 170:132–137. https://doi.org/10.1007/s002030050624

    Article  CAS  PubMed  Google Scholar 

  36. Nishino SF, Spain JC (1993) Degradation of nitrobenzene by a Pseudomonas pseudoalcaligenes. Appl Environ Microbiol 59:2520–2525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Panas P, Ternan NG, Dooley JSG, McMullan G (2006) Detection of phosphonoacetate degradation and phnA genes in soil bacteria from distinct geographical origins suggest its possible biogenic origin. Environ Microbiol 8:939–945. https://doi.org/10.1111/j.1462-2920.2005.00974.x

    Article  CAS  PubMed  Google Scholar 

  38. Kulakova AN, Kulakov LA, Quinn JP (1997) Cloning of the phosphonoacetate hydrolase gene from Pseudomonas fluorescens 23F encoding a new type of carbon–phosphorus bond cleaving enzyme and its expression in Escherichia coli and Pseudomonas putida. Gene 195:49–53. https://doi.org/10.1016/S0378-1119(97)00151-0

    Article  CAS  PubMed  Google Scholar 

  39. McMullan G, Harrington F, Quinn JP (1992) Metabolism of phosphonoacetate as the sole carbon and phosphorus source by an environmental bacterial isolate. Appl Environ Microbiol 58:1364–1366. https://doi.org/10.1128/AEM.58.4.1364-1366.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dolan SK, Wijaya A, Geddis SM et al (2018) Loving the poison: the methylcitrate cycle and bacterial pathogenesis. Microbiol (United Kingdom) 164:251–259. https://doi.org/10.1099/mic.0.000604

    Article  CAS  Google Scholar 

  41. Zarzycki J, Fuchs G (2011) Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl Environ Microbiol 77:6181–6188. https://doi.org/10.1128/AEM.00705-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Grostern A, Sales CM, Zhuang WQ et al (2012) Glyoxylate metabolism is a key feature of the metabolic degradation of 1,4-dioxane by Pseudonocardia dioxanivorans strain CB1190. Appl Environ Microbiol 78:3298–3308. https://doi.org/10.1128/AEM.00067-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kornberg H, Morris J (1965) The Utilization of glycollate by micrococcus denitrificans: the β-hydroxyaspartate pathway. Biochem J 95:577–586. https://doi.org/10.1042/bj0950577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Pelz O, Tesar M, Wittich RM et al (1999) Towards elucidation of microbial community metabolic pathways: unravelling the network of carbon sharing in a pollutant-degrading bacterial consortium by immunocapture and isotopic ratio mass spectrometry. Environ Microbiol 1:167–174. https://doi.org/10.1046/j.1462-2920.1999.00023.x

    Article  CAS  PubMed  Google Scholar 

  45. Wongkittchote P, Mew N, Chapman K (2017) Propionyl-CoA carboxylase—a review. Mol Genet Metab 122:145–152. https://doi.org/10.1016/j.ymgme.2017.10.002

    Article  CAS  Google Scholar 

  46. Shi L, Tu BP (2015) Acetyl-CoA and the regulation of metabolism: mechanisms and consequences. Curr Opin Cell Biol 33:125–131. https://doi.org/10.1016/j.ceb.2015.02.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Nygaard P (2014) Purine and pyrimidine salvage pathways. Bacillus subtilis and other Gram-positive bacteria. ASM Press, Washington, D.C., pp 359–378

    Chapter  Google Scholar 

  48. Booth IR, Kroll RG (1983) Regulation of cytoplasmic pH (pH1) in bacteria and its relationship to metabolism. Biochem Soc Trans 11:70–72. https://doi.org/10.1042/bst0110070

    Article  CAS  PubMed  Google Scholar 

  49. Blomqvist K, Nikkola M, Lehtovaara P et al (1993) Characterization of the genes of the 2,3-butanediol operons from Klebsiella terrigena and Enterobacter aerogenes. J Bacteriol 175:1392–1404. https://doi.org/10.1128/jb.175.5.1392-1404.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Scolnik PA, Walker MA, Marrs BL (1980) Biosynthesis of carotenoids derived from neurosporene in Rhodopseudomonas capsulata. J Biol Chem 255:2427–2432

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the Technical University of Liberec within the project “Environmental fate, behaviour and biological effects of engineered nanomaterials” Project No. 30001. The authors acknowledge the assistance provided by the Research Infrastructures NanoEnviCz (Project No. LM2018124) and Pro-NanoEnviCz (Project No. CZ.02.1.01/0.0/0.0/16_013/0001821), supported by the Ministry of Education, Youth and Sports of the Czech Republic.

Author information

Authors and Affiliations

  1. Institute for Nanomaterials, Advanced Technologies and Innovation, Technical University of Liberec (TUL), Studentská 2, 46117, Liberec, Czech Republic

    Nhung H. A. Nguyen, Roman Špánek & Alena Ševců

  2. Faculty of Mechatronics, Informatics and Interdisciplinary Studies, Technical University of Liberec (TUL), Studentská 2, 46117, Liberec, Czech Republic

    Roman Špánek

  3. Department of Chemistry, University of Illinois at Urbana-Champaign, 600 South Mathews Avenue, Urbana, IL, 61801, USA

    Priscila Falagan-Lotsch

  4. Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA

    Priscila Falagan-Lotsch

Authors
  1. Nhung H. A. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roman Špánek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Priscila Falagan-Lotsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alena Ševců
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NHAN and AŠ designed the original experiment published in Nguyen et al. 2018. NHAN. Wrote most of the manuscript. RŠ performed bioinformatic analysis of 16S rRNA sequences and participated in writing the manuscript. PFL advised on shaping the article, and together with AŠ, corrected the text. NHAN and RŠ contributed equally to this article.

Corresponding authors

Correspondence to Nhung H. A. Nguyen, Roman Špánek or Alena Ševců.

Ethics declarations

Conflict of interest

The authors declare no financial competition or interests in relation to the work described.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 331 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, N.H.A., Špánek, R., Falagan-Lotsch, P. et al. Impact of Zero-Valent Iron on Freshwater Bacterioplankton Metabolism as Predicted from 16S rRNA Gene Sequence Libraries. Curr Microbiol 78, 979–991 (2021). https://doi.org/10.1007/s00284-021-02362-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-021-02362-7

Search

Navigation