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Applied Microbiology and Biotechnology

, Volume 102, Issue 23, pp 10299–10314 | Cite as

Biodegradation of sulfamethoxazole by a bacterial consortium of Achromobacter denitrificans PR1 and Leucobacter sp. GP

  • Ana C. Reis
  • Monika Čvančarová
  • Ying Liu
  • Markus Lenz
  • Timm Hettich
  • Boris A. Kolvenbach
  • Philippe F.-X. Corvini
  • Olga C. Nunes
Environmental biotechnology

Abstract

In the last decade, biological degradation and mineralization of antibiotics have been increasingly reported feats of environmental bacteria. The most extensively described example is that of sulfonamides that can be degraded by several members of Actinobacteria and Proteobacteria. Previously, we reported sulfamethoxazole (SMX) degradation and partial mineralization by Achromobacter denitrificans strain PR1, isolated from activated sludge. However, further studies revealed an apparent instability of this metabolic trait in this strain. Here, we investigated this instability and describe the finding of a low-abundance and slow-growing actinobacterium, thriving only in co-culture with strain PR1. This organism, named GP, shared highest 16S rRNA gene sequence similarity (94.6–96.9%) with the type strains of validly described species of the genus Leucobacter. This microbial consortium was found to harbor a homolog to the sulfonamide monooxygenase gene (sadA) also found in other sulfonamide-degrading bacteria. This gene is overexpressed in the presence of the antibiotic, and evidence suggests that it codes for a group D flavin monooxygenase responsible for the ipso-hydroxylation of SMX. Additional side reactions were also detected comprising an NIH shift and a Baeyer–Villiger rearrangement, which indicate an inefficient biological transformation of these antibiotics in the environment. This work contributes to further our knowledge in the degradation of this ubiquitous micropollutant by environmental bacteria.

Keywords

Bacterial consortium Sulfonamide Mass spectra Metabolic pathway Ipso-hydroxylation 16S rRNA gene Nanopore sequencing 

Notes

Acknowledgments

The authors wish to thank Anna Weston (FHNW, Switzerland) for the advice on the optimization of the qPCR assays, Jonas Romer (FHNW, Switzerland) for the assistance with the TiO2/UV experiments, Prof. Dr. Hans-Peter Kohler (EWAG, Switzerland) for the helpful insights about the metabolic pathway, and Dr. Ana Rita Lopes (FEUP, Portugal) for the relevant comments about the structure of the manuscript and presentation of results. The authors wish to acknowledge the Swiss National Science Foundation, Comissão de Coordenação e Desenvolvimento Regional do Norte and Fundação para a Ciência e a Tecnologia for the funding. Ana Reis further acknowledges the Fundação para a Ciência e a Tecnologia (FCT) for her PhD scholarship.

Funding

This work was financially supported by the Swiss National Science Foundation (grant no. 160332), Comissão de Coordenação e Desenvolvimento Regional do Norte (project reference NORTE-01-0145-FEDER-000005), and Fundação para a Ciência e a Tecnologia and Technology (FCT) through the project UID/EQU/00511/2013—POCI-01-0145-FEDER-006939 and Ana Reis PhD grant (reference SFRH/BD/95814/2013).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2018_9411_MOESM1_ESM.pdf (1.6 mb)
ESM 1 (PDF 1657 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ana C. Reis
    • 1
    • 2
  • Monika Čvančarová
    • 2
  • Ying Liu
    • 2
  • Markus Lenz
    • 2
  • Timm Hettich
    • 3
  • Boris A. Kolvenbach
    • 2
  • Philippe F.-X. Corvini
    • 2
  • Olga C. Nunes
    • 1
  1. 1.LEPABE—Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, Department of Chemical EngineeringUniversity of PortoPortoPortugal
  2. 2.Institute for Ecopreneurship, School of Life SciencesUniversity of Applied Sciences Northwestern SwitzerlandMuttenzSwitzerland
  3. 3.Institute for Chemistry and Bioanalytics, School of Life SciencesUniversity of Applied Sciences Northwestern SwitzerlandMuttenzSwitzerland

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