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Catabolism of the groundwater micropollutant 2,6-dichlorobenzamide beyond 2,6-dichlorobenzoate is plasmid encoded in Aminobacter sp. MSH1

  • Jeroen T’Syen
  • Bart Raes
  • Benjamin Horemans
  • Raffaella Tassoni
  • Baptiste Leroy
  • Cédric Lood
  • Vera van Noort
  • Rob Lavigne
  • Ruddy Wattiez
  • Hans-Peter E. Kohler
  • Dirk Springael
Applied genetics and molecular biotechnology

Abstract

Aminobacter sp. MSH1 uses the groundwater micropollutant 2,6-dichlorobenzamide (BAM) as sole source of carbon and energy. In the first step, MSH1 converts BAM to 2,6-dichlorobenzoic acid (2,6-DCBA) by means of the BbdA amidase encoded on the IncP-1β plasmid pBAM1. Information about the genes and degradation steps involved in 2,6-DCBA metabolism in MSH1 or any other organism is currently lacking. Here, we show that the genes for 2,6-DCBA degradation in strain MSH1 reside on a second catabolic plasmid in MSH1, designated as pBAM2. The complete sequence of pBAM2 was determined revealing that it is a 53.9 kb repABC family plasmid. The 2,6-DCBA catabolic genes on pBAM2 are organized in two main clusters bordered by IS elements and integrase genes and encode putative functions like Rieske mono-/dioxygenase, meta-cleavage dioxygenase, and reductive dehalogenases. The putative mono-oxygenase encoded by the bbdD gene was shown to convert 2,6-DCBA to 3-hydroxy-2,6-dichlorobenzoate (3-OH-2,6-DCBA). 3-OH-DCBA was degraded by wild-type MSH1 and not by a pBAM2-free MSH1 variant indicating that it is a likely intermediate in the pBAM2-encoded DCBA catabolic pathway. Based on the activity of BbdD and the putative functions of the other catabolic genes on pBAM2, a metabolic pathway for BAM/2,6-DCBA in strain MSH1 was suggested.

Keywords

2,6-Dichlorobenzamide Catabolic pathway Plasmid encoded Aminobacter Drinking water treatment 

Notes

Acknowledgements

The authors thank J. Aamand for providing strains MSH1, ASI1, and ASI2; Dianne K. Newman for providing E. coli BW29427, A. Provoost for skillful help in plasmid isolation, M. Everaert for lyophilization, T. Fleischmann and I. Schilling for helping with HPLC-MS and identification of 3-OH-2,6-DCBA, and J. Cornelis for technical assistance.

Funding

This work was supported by IWT-Vlaanderen Strategic Basic Research project [grant number 101589], the Inter-University Attraction Pole (IUAP) “μ-manager” of the Belgian Science Policy (BELSPO) [grant number P7/25], EU project BIOTREAT [EU grant number 266039] and by the FNRS under grant “grand equipment” [grant number2877824]. CL was supported by an SB PhD fellowship [grant number 1S64718N] and BH by a postdoctoral fellowship [grant number12Q0218N] from FWO Vlaanderen.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical statement

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

Supplementary material

253_2018_9189_MOESM1_ESM.pdf (411 kb)
ESM 1 (PDF 411 kb)

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Copyright information

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

Authors and Affiliations

  • Jeroen T’Syen
    • 1
  • Bart Raes
    • 1
  • Benjamin Horemans
    • 1
  • Raffaella Tassoni
    • 1
  • Baptiste Leroy
    • 2
  • Cédric Lood
    • 3
    • 4
  • Vera van Noort
    • 3
  • Rob Lavigne
    • 4
  • Ruddy Wattiez
    • 2
  • Hans-Peter E. Kohler
    • 5
  • Dirk Springael
    • 1
  1. 1.Division of Soil and Water ManagementKU LeuvenLeuvenBelgium
  2. 2.Department of Proteomics and Microbiology, Research Institute for BiosciencesUniversity of MonsMonsBelgium
  3. 3.Centre of Microbial and Plant Genetics, Department of Microbial and Molecular SystemsKU LeuvenLeuvenBelgium
  4. 4.Laboratory of Gene TechnologyKU LeuvenLeuvenBelgium
  5. 5.Department of Environmental MicrobiologySwiss Federal Institute of Aquatic Science and Technology (EAWAG)DübendorfSwitzerland

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