Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Identification of a virulent phage infecting species of Nitrosomonas

Abstract

In the first and limiting step of nitrification, ammonia (NH3) is oxidised to nitrite (NO2) by the action of some prokaryotes, including bacteria of the Nitrosomonas genus. A potential approach to nitrification inhibition would be through the application of phages, but until now this method has been unexplored and no virulent phages that infect nitrifying bacteria have been described. In this study, we report the isolation of the first phage infecting some Nitrosomonas species. This polyvalent virulent phage (named ΦNF-1) infected Nitrosomonas europaea, Nitrosomonas communis, and Nitrosomonas nitrosa. Phage ΦNF-1 has the morphology of the Podoviridae family, a dsDNA genome of 41,596 bp and a 45.1 % GC content, with 50 predicted open reading frames. Phage ΦNF-1 was found to inhibit bacterial growth and reduce NH4+ consumption in the phage-treated cultures. The application of phages as biocontrol agents could be a useful strategy for nitrification inhibition without the restrictions associated with chemical inhibitors.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Growth of Nitrosomonas cultures in the presence of phage ΦNF-1 and the effect of the phage on the NH4+ uptake in the cultures.
Fig. 2: Morphological and genetic characterization of phage ΦNF-1.

Similar content being viewed by others

Data availability

All data are available in the main text or the supplementary online materials. The phage genome is available at GenBank accession number OL634959.

References

  1. van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op Den Camp HJM, Kartal B, et al. Complete nitrification by a single microorganism. Nature. 2015;528:555–9.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Rowan AK, Snape JR, Fearnside D, Barer MR, Curtis TP, Head IM. Composition and diversity of ammonia-oxidising bacterial communities in wastewater treatment reactors of different design treating identical wastewater. FEMS Microbiol Ecol. 2003;43:195–206.

    Article  CAS  PubMed  Google Scholar 

  3. de Boer W, Kowalchuk GA. Nitrification in acid soils: microorganisms and mechanisms. Soil Biol Biochem. 2001;33:853–66.

    Article  Google Scholar 

  4. Carberry PS, Liang W, Twomlow S, Holzworth DP, Dimes JP, McClelland T, et al. Scope for improved eco-efficiency varies among diverse cropping systems. Proc Natl Acad Sci USA 2013;110:8381–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Stein LY, Klotz MG. The nitrogen cycle. Curr Biol. 2016;26:R94–R98.

    Article  CAS  PubMed  Google Scholar 

  6. Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, et al. Suppression of soil nitrification by plants. Plant Sci. 2015;233:155–64.

    Article  CAS  PubMed  Google Scholar 

  7. Hertwig S, Hammerl JA, Appel B, Alter T. Post-harvest application of lytic bacteriophages for biocontrol of foodborne pathogens and spoilage bacteria. Berl Munch Tierarzt Wochenschr. 2013;126:357–69.

    Google Scholar 

  8. Svircev A, Roach D, Castle A. Framing the future with bacteriophages in agriculture. Viruses. 2018;10:218.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Iriarte FB, Obradović A, Wernsing MH, Jackson LE, Balogh B, Hong JA, et al. Soil-based systemic delivery and phyllosphere in vivo propagation of bacteriophages. Bacteriophage. 2012;2:e23530.

    Article  Google Scholar 

  10. Greer GG. Bacteriophage control of foodborne bacteria. J Food Prot. 2005;68:1102–11.

    Article  PubMed  Google Scholar 

  11. Vázquez R, Díez-Martínez R, Domingo-Calap P, García P, Gutiérrez D, Muniesa M, et al. Essential topics for the regulatory consideration of phages as clinically valuable therapeutic agents: a perspective from Spain. Microorganisms. 2022;10:717.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Krom MD. Spectrophotometric determination of ammonia: A study of a modified berthelot reaction using salicylate and dichloroisocyanurate. Analyst. 1980;105:305–16.

    Article  CAS  Google Scholar 

  13. Kempers AJ, Zweers A. Ammonium determination in soil extracts by the salicylate method. Commun Soil Sci Plant Anal. 2008;17:715–23.

    Article  Google Scholar 

  14. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, Elsevier/ Academic Press, San Diego, 2011.

  15. Choi J, Kotay SM, Goel R. Various physico-chemical stress factors cause prophage induction in Nitrosospira multiformis 25196-an ammonia oxidizing bacteria. Water Res. 2010;44:4550–8.

    Article  CAS  PubMed  Google Scholar 

  16. Kim JG, Kim SJ, Cvirkaite-Krupovic V, Yu WJ, Gwak JH, López-Pérez M, et al. Spindle-shaped viruses infect marine ammoniaoxidizing thaumarchaea. Proc Natl Acad Sci USA. 2019;116:15645–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kösler JE, Calvo OC, Franzaring J, Fangmeier A. Evaluating the ecotoxicity of nitrification inhibitors using terrestrial and aquatic test organisms. Environ Sci Eur. 2019;31:91.

    Article  Google Scholar 

  18. Scheurer M, Brauch H-J, Schmidt CK, Sacher F. Occurrence and fate of nitrification and urease inhibitors in the aquatic environment. Environ Sci Process Impacts. 2016;18:999–1010.

    Article  CAS  PubMed  Google Scholar 

  19. Abalos D, Jeffery S, Sanz-Cobena A, Guardia G, Vallejo A. Meta-analysis of the effect of urease and nitrification inhibitors on crop productivity and nitrogen use efficiency. Agric Ecosyst Environ. 2014;189:136–44.

    Article  CAS  Google Scholar 

  20. Kahn LH, Bergeron G, Bourassa MW, De Vegt B, Gill J, Gomes F, et al. From farm management to bacteriophage therapy: strategies to reduce antibiotic use in animal agriculture. Ann N Y Acad Sci. 2019;1441:31–9.

  21. Reardon S. Phage therapy gets revitalized. Nature. 2014;510:15–6.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Spanish Ministerio de Ciencia e Innovación (PID2020-113355GB-I00, the Agencia Estatal de Investigación (AEI) and the European regional fund (ERF), and the CDTI project (IDI-20190017). The study was partially supported by the Generalitat de Catalunya (2017SGR170). L. R.-R is lecturer of the Serra-Hunter program, Generalitat de Catalunya. C. G-G. has a fellowship from the University of Barcelona. L. S-C has a Maria Zambrano fellowship from the Spanish Ministerio de Universidades. M.D.R-B has a Margarita Salas fellowship from the Spanish Ministerio de Universidades.

Author information

Authors and Affiliations

Authors

Contributions

PQ, LSC, CGG, GV, TYC, SGG, SGM performed the experiments, MDRB and LRR performed sequencing analysis, PQ, SA, AV, IS and MM conceived and funded the study, designed the experiments, and wrote the paper.

Corresponding author

Correspondence to Maite Muniesa.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quirós, P., Sala-Comorera, L., Gómez-Gómez, C. et al. Identification of a virulent phage infecting species of Nitrosomonas. ISME J 17, 645–648 (2023). https://doi.org/10.1038/s41396-023-01380-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41396-023-01380-6

Search

Quick links