Environmental Science and Pollution Research

, Volume 24, Issue 1, pp 52–65 | Cite as

Bacterial host and reporter gene optimization for genetically encoded whole cell biosensors

  • Catherine Brutesco
  • Sandra Prévéral
  • Camille Escoffier
  • Elodie C. T. Descamps
  • Elsa Prudent
  • Julien Cayron
  • Louis Dumas
  • Manon Ricquebourg
  • Géraldine Adryanczyk-Perrier
  • Arjan de Groot
  • Daniel Garcia
  • Agnès Rodrigue
  • David Pignol
  • Nicolas Ginet
In-line Multiplexed Biosensing

Abstract

Whole-cell biosensors based on reporter genes allow detection of toxic metals in water with high selectivity and sensitivity under laboratory conditions; nevertheless, their transfer to a commercial inline water analyzer requires specific adaptation and optimization to field conditions as well as economical considerations. We focused here on both the influence of the bacterial host and the choice of the reporter gene by following the responses of global toxicity biosensors based on constitutive bacterial promoters as well as arsenite biosensors based on the arsenite-inducible Pars promoter. We observed important variations of the bioluminescence emission levels in five different Escherichia coli strains harboring two different lux-based biosensors, suggesting that the best host strain has to be empirically selected for each new biosensor under construction. We also investigated the bioluminescence reporter gene system transferred into Deinococcus deserti, an environmental, desiccation- and radiation-tolerant bacterium that would reduce the manufacturing costs of bacterial biosensors for commercial water analyzers and open the field of biodetection in radioactive environments. We thus successfully obtained a cell survival biosensor and a metal biosensor able to detect a concentration as low as 100 nM of arsenite in D. deserti. We demonstrated that the arsenite biosensor resisted desiccation and remained functional after 7 days stored in air-dried D. deserti cells. We also report here the use of a new near-infrared (NIR) fluorescent reporter candidate, a bacteriophytochrome from the magnetotactic bacterium Magnetospirillum magneticum AMB-1, which showed a NIR fluorescent signal that remained optimal despite increasing sample turbidity, while in similar conditions, a drastic loss of the lux-based biosensors signal was observed.

Keywords

Arsenite biosensor Bioluminescence Near-infrared fluorescent reporter Deinococcus deserti Desiccation Bacteriophytochrome 

Notes

Acknowledgments

This work was funded by the French national research agency ANR on the call-for-project ECOTECH (project COMBITOX, ANR-11-ECOT-0009) and also supported by the Centre National de la Recherche Scientifique and the Commissariat à l’Énergie Atomique et aux Énergies Alternatives (program NRBC). We thank all the members of the COMBITOX project for fruitful discussions and interactions. We also thank Dr. Eric Giraud for the kind gift of the PPΦ3295 plasmid.

References

  1. Ansaldi M, Bazin I, Cholat P et al (2015) Toward inline multiplex biodetection of metals, bacteria, and toxins in water networks: the COMBITOX project. Environ Sci Pollut Res Int. doi:10.1007/s11356-015-5582-4 Google Scholar
  2. Cayron J, Prudent E, Escoffier C et al (2015) Pushing the limits of nickel detection to nanomolar range using a set of engineered bioluminescent Escherichia coli. Environ Sci Pollut Res Int. doi:10.1007/s11356-015-5580-6 Google Scholar
  3. de Groot A, Chapon V, Servant P et al (2005) Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert. Int J Syst Evol Microbiol 55:2441–2446. doi:10.1099/ijs.0.63717-0 CrossRefGoogle Scholar
  4. de Groot A, Dulermo R, Ortet P et al (2009) Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet 5:e1000434. doi:10.1371/journal.pgen.1000434 CrossRefGoogle Scholar
  5. de Groot A, Roche D, Fernandez B et al (2014) RNA sequencing and proteogenomics reveal the importance of leaderless mRNAs in the radiation-tolerant bacterium Deinococcus deserti. Genome Biol Evol 6:932–948. doi:10.1093/gbe/evu069 CrossRefGoogle Scholar
  6. Dulermo R, Fochesato S, Blanchard L, de Groot A (2009) Mutagenic lesion bypass and two functionally different RecA proteins in Deinococcus deserti. Mol Microbiol 74:194–208. doi:10.1111/j.1365-2958.2009.06861.x CrossRefGoogle Scholar
  7. Giraud E, Verméglio A (2008) Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosynth Res 97:141–153. doi:10.1007/s11120-008-9323-0 CrossRefGoogle Scholar
  8. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130CrossRefGoogle Scholar
  9. Hayashi K, Morooka N, Yamamoto Y et al (2006) Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2:2006.0007. doi:10.1038/msb4100049 CrossRefGoogle Scholar
  10. Hynninen A, Virta M (2010) Whole-cell bioreporters for the detection of bioavailable metals. Adv Biochem Eng Biotechnol 118:31–63. doi:10.1007/10_2009_9 Google Scholar
  11. Magrisso S, Erel Y, Belkin S (2008) Microbial reporters of metal bioavailability. Microb Biotechnol 1:320–330. doi:10.1111/j.1751-7915.2008.00022.x CrossRefGoogle Scholar
  12. Matsunaga T, Okamura Y, Fukuda Y et al (2005) Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Res Int J Rapid Publ Rep Genes Genomes 12:157–166. doi:10.1093/dnares/dsi002 Google Scholar
  13. Norrander J, Kempe T, Messing J (1983) Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101–106CrossRefGoogle Scholar
  14. Peng Z, Yan Y, Xu Y et al (2010) Improvement of an E. coli bioreporter for monitoring trace amounts of phenol by deletion of the inducible σ54-dependent promoter. Biotechnol Lett 32:1265–1270. doi:10.1007/s10529-010-0317-6 CrossRefGoogle Scholar
  15. Prévéral S, Brutesco C, Descamps ECT et al (2016) A bioluminescent arsenite biosensor designed for inline water analyzer. Environ Sci Pollut Res Int. doi:10.1007/s11356-015-6000-7 Google Scholar
  16. Rose RE (1988) The nucleotide sequence of pACYC184. Nucleic Acids Res 16:355CrossRefGoogle Scholar
  17. Sharrock RA (2008) The phytochrome red/far-red photoreceptor superfamily. Genome Biol 9:230. doi:10.1186/gb-2008-9-8-230 CrossRefGoogle Scholar
  18. Shu X, Royant A, Lin MZ et al (2009) Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324:804–807. doi:10.1126/science.1168683 CrossRefGoogle Scholar
  19. Sun J-Z, Peter Kingori G, Si R-W et al (2015) Microbial fuel cell-based biosensors for environmental monitoring: a review. Water Sci Technol J Int Assoc Water Pollut Res 71:801–809. doi:10.2166/wst.2015.035 CrossRefGoogle Scholar
  20. Vallenet D, Labarre L, Rouy Z et al (2006) MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res 34:53–65. doi:10.1093/nar/gkj406 CrossRefGoogle Scholar
  21. Vinay M, Franche N, Grégori G et al (2015) Phage-based fluorescent biosensor prototypes to specifically detect enteric bacteria such as E. coli and Salmonella enterica Typhimurium. PLoS One 10:e0131466. doi:10.1371/journal.pone.0131466 CrossRefGoogle Scholar
  22. Winson MK, Swift S, Hill PJ et al (1998) Engineering the luxCDABE genes from Photorhabdus luminescens to provide a bioluminescent reporter for constitutive and promoter probe plasmids and mini-Tn5 constructs. FEMS Microbiol Lett 163:193–202CrossRefGoogle Scholar
  23. Xiong A-S, Peng R-H, Zhuang J et al (2012) Advances in directed molecular evolution of reporter genes. Crit Rev Biotechnol 32:133–142. doi:10.3109/07388551.2011.593503 CrossRefGoogle Scholar
  24. Xu T, Close DM, Sayler GS, Ripp S (2013) Genetically modified whole-cell bioreporters for environmental assessment. Ecol Indic 28:125–141. doi:10.1016/j.ecolind.2012.01.020 CrossRefGoogle Scholar
  25. Yagur-Kroll S, Belkin S (2010) Upgrading bioluminescent bacterial bioreporter performance by splitting the lux operon. Anal Bioanal Chem 400:1071–1082. doi:10.1007/s00216-010-4266-7 CrossRefGoogle Scholar
  26. Yagur-Kroll S, Belkin S (2014) Molecular manipulations for enhancing luminescent bioreporters performance in the detection of toxic chemicals. Adv Biochem Eng Biotechnol 145:137–149. doi:10.1007/978-3-662-43619-6_4 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Catherine Brutesco
    • 1
    • 2
    • 3
  • Sandra Prévéral
    • 1
    • 2
    • 3
  • Camille Escoffier
    • 1
    • 2
    • 3
  • Elodie C. T. Descamps
    • 1
    • 2
    • 3
  • Elsa Prudent
    • 4
    • 5
    • 6
  • Julien Cayron
    • 4
    • 5
    • 6
  • Louis Dumas
    • 1
    • 2
    • 3
  • Manon Ricquebourg
    • 1
    • 2
    • 3
  • Géraldine Adryanczyk-Perrier
    • 1
    • 2
    • 3
  • Arjan de Groot
    • 1
    • 2
    • 3
  • Daniel Garcia
    • 1
    • 2
    • 3
  • Agnès Rodrigue
    • 4
    • 5
    • 6
  • David Pignol
    • 1
    • 2
    • 3
  • Nicolas Ginet
    • 1
    • 2
    • 3
  1. 1.CEA, DRF, BIAM, Lab Bioenerget CellulaireSaint-Paul-lez-DuranceFrance
  2. 2.CNRS, UMR Biol Veget and Microbiol EnvironSaint-Paul-lez-DuranceFrance
  3. 3.Aix-Marseille UniversitéSaint-Paul-lez-DuranceFrance
  4. 4.Université de LyonLyonFrance
  5. 5.INSA de LyonVilleurbanneFrance
  6. 6.CNRS, UMR5240, Microbiologie, Adaptation et PathogénieVilleurbanneFrance

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