Advertisement

Nitrate levels modulate the abundance of Paracoccus sp. in a biofilm community

Abstract

Conditions required to enhance a particular species efficient in degradative capabilities is very useful in wastewater treatment processes. Paracoccus sp. is known to efficiently reduce nitrogen oxides (NOx) due to the branched denitrification pathway. Individual-based simulations showed that the relative fitness of Paracoccus sp. to Pseudomonas sp. increased significantly with nitrate levels above 5 mM. Spatial structure of the biofilm showed substantially less nitrite levels in the areas of Paracoccus sp. dominance. The simulation was validated in a laboratory reactor harboring biofilm community by fluorescent in situ hybridization, which showed that increasing nitrate levels enhanced the abundance of Paracoccus sp. Different levels of NOx did not display any significant effect on biofilm formation of Paracoccus sp., unlike several other bacteria. This study shows that the attribute of Paracoccus sp. to tolerate and efficiently reduce NOx is conferring a fitness payoff to the organism at high concentrations of nitrate in a multispecies biofilm community.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3

References

  1. Almeida JS, Julio SM, Reis MAM, Carrondo MJT (1995) Nitrite inhibition of denitrification by Pseudomonas fluorescens. Biotech Bioeng 46:194–201

  2. Barraud N, Hassett DJ, Hwang S-H, Rice SA, Kjelleberg S, Webb JS (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344–7353

  3. Barraud N, Webb JS, Storey MV, Rice SA, Kjelleberg S (2009) Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2:370–378

  4. Betlach MR, Tiedje JM (1981) Kinetic explanation for accumulation of nitrite, nitric oxide, and nitrous oxide during bacterial denitrification. Appl Environ Microbiol 42:1074–1084

  5. Carlson CA, Ingraham JL (1983) Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans. Appl Environ Microbiol 45:1247–1253

  6. Chakravarthy SS, Pande S, Kapoor A, Nerurkar AS (2011) Comparison of denitrification between Paracoccus sp. and Diaphorobacter sp. Appl Biochem Biotech 165:260–269

  7. Costerton JW, Lewandowski Z, DeBeer D, Calwell D, Korber D, James G (1994) Biofilms, the customized microniche. J Bacteriol 176:2137–2142

  8. Daims H, Stoecker K, Wagner M (2005) Flourescence in situ hybridization for the detection of prokaryotes. In: Smith C, Osborn M (eds) Molecular microbial ecology. Taylor & Francis, New York, pp 213–239

  9. Fernandez-Nava Y, Maranon E, Soons J, Castrillon L (2008) Denitrification of wastewater containing high nitrate and calcium concentrations. Bioresour Technol 99:7976–7981

  10. Hallin S, Rothman M, Pell M (1996) Adaptation of denitrifying bacteria to acetate and methanol in activated sludge. Water Res 30:1445–1450

  11. Hao X, Loosdrecht MCMV, Meijer SC, Qian Y (2001) Model-based evaluation of two BNR processes UCT and A2N. Water Res 35:2851–2860

  12. Horn H, Neu TR, Wulkow M (2001) Modelling the structure and function of extracellular polymeric substances in biofilms with new numerical techniques. Water Sci Technol 43:121–127

  13. Kucera I, Dadak V, Dobry R (1983) The Distribution of redox equivalents in the anaerobic respiratory chain of Paracoccus denitrificans. Eur J Biochem 130:359–364

  14. Lardon LA, Merkey BV, Martins S, Dötsch A, Picioreanu C, Kreft J-U, Smets BF (2011) iDynoMiCS: next-generation individual-based modelling of biofilms. Environ Microbiol 13:2416–2434

  15. Lenski RE, Rose MR, Simpson SC, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2000 generations. Am Nat 138:1315–1341

  16. Neef A, Zaglauer A, Meier H, Amann R, Lemeer H, Schleifer K-H (1996) Population analysis in a denitrifying sand filter: conventional and in situ Identification of Paracoccus spp. in methanol-fed biofilms. Appl Environ Microbiol 62:4329–4339

  17. Nicolella C, Loosdrecht MCMV, Heijnen JJ (2000) Wastewater treatment with particulate biofilm reactors. J Biotechnol 80:1–33

  18. Osaka T, Shirotani K, Yoshie S, Tsuneda S (2008) Effects of carbon source on denitrification efficiency and microbial community structure in a saline wastewater treatment process. Water Res 42:3709–3718

  19. Qureshi N, Annous BA, Ezeji TC, Karcher P, Maddox IS (2005) Biofilm reactors for industrial bioconversion processes: employing potential of enhanced reaction rates. Microb Cell Fact 4:1–21

  20. Schlag S, Nerz C, Birkenstock TA, Altenberend F, Götz F (2007) Inhibition of Staphylococcal biofilm formation by nitrite. J Bacteriol 189:7911–7919

  21. Srinandan CS, Jadav V, Cecilia D, Nerurkar AS (2010) Nutrients determine the spatial architecture of Paracoccus sp. biofilm. Biofouling 26:449–459

  22. Srinandan CS, Shah M, Patel B, Nerurkar AS (2011) Assessment of denitrifying bacterial composition in activated sludge. Bioresour Tech 102:9481–9489

  23. Srinandan CS, D’souza G, Srivastava N, Nayak BB (2012) Carbon sources influence the nitrate removal activity, community structure and biofilm architecture. Bioresour Technol 117:292–299

  24. Strohm TO, Griffin B, Zumft WG, Schink B (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73:1420–1424

  25. Watt M, Hugenholtz P, White R, Vinall K (2006) Numbers and locations of native bacteria on field-grown wheat roots quantified by fluorescence in situ hybridization (FISH). Environ Microbiol 8:871–884

  26. Wiesmann U (1994) Biological nitrogen removal from wastewater. Biochem Eng Biotech 51:113–154

  27. Xavier JB, Foster KR (2007) Cooperation and conflict in microbial biofilms. Proc Nat Acad Sci 104:876–881

  28. Xavier J, Picioreanu C, Loosdrecht MCMV (2005) A framework for multidimensional modelling of activity and structure of multispecies biofilms. Environ Microbiol 7:1085–1103

Download references

Acknowledgments

The authors would like to thank J-U Kreft and Rob Clegg, Univ. of Birmingham for help in troubleshooting iDynoMICS. Namrata Acharya, M. S Univ. for assisting in FISH experiments is acknowledged. The work was supported by Prof. T. R. Rajagopalan fund, SASTRA University.

Author information

Correspondence to C. S. Srinandan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MP4 832 kb)

Supplementary material 2 (MP4 1112 kb)

Supplementary material 3 (MP4 1080 kb)

Supplementary material 4 (MP4 900 kb)

Supplementary material 5 (MP4 967 kb)

Supplementary material 6 (MP4 885 kb)

Supplementary material 7 (MP4 850 kb)

Supplementary material 8 (MP4 1002 kb)

Supplementary material 1 (MP4 832 kb)

Supplementary material 2 (MP4 1112 kb)

Supplementary material 3 (MP4 1080 kb)

Supplementary material 4 (MP4 900 kb)

Supplementary material 5 (MP4 967 kb)

Supplementary material 6 (MP4 885 kb)

Supplementary material 7 (MP4 850 kb)

Supplementary material 8 (MP4 1002 kb)

Supplementary material 9 (DOCX 606 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Singh, S., Nerurkar, A.S. & Srinandan, C.S. Nitrate levels modulate the abundance of Paracoccus sp. in a biofilm community. World J Microbiol Biotechnol 31, 951–958 (2015). https://doi.org/10.1007/s11274-015-1849-7

Download citation

Keywords

  • Denitrification
  • Nitrate removal
  • Biofilm community
  • Paracoccus
  • Pseudomonas