Advertisement

Antonie van Leeuwenhoek

, Volume 99, Issue 3, pp 489–499 | Cite as

Description of Citricoccus nitrophenolicus sp. nov., a para-nitrophenol degrading actinobacterium isolated from a wastewater treatment plant and emended description of the genus Citricoccus Altenburger et al. 2002

  • Marie Bank Nielsen
  • Kasper Urup Kjeldsen
  • Kjeld IngvorsenEmail author
Original Paper

Abstract

A novel actinobacterium, designated PNP1T, was isolated from a wastewater treatment plant at a pesticide factory by selective enrichment with para-nitrophenol. The strictly aerobic strain PNP1T grew with para-nitrophenol as the sole carbon and energy source. Metabolism of para-nitrophenol resulted in the stoichiometric release of nitrite. When incubated with both para-nitrophenol and acetate, para-nitrophenol was degraded and utilized as growth substrate prior to acetate. When grown on acetate (in the absence of ammonium) both nitrite and nitrate served as nitrogen sources, nitrate being quantitatively reduced to nitrite which accumulated in cultures during aerobic growth. Cells were coccoid and stained Gram-positive, were non-motile and did not form endospores. Colonies of strain PNP1T on agar medium were bright yellow, circular and smooth. The dominant menaquinone was MK-8(H2) (54%) and the major cellular fatty acid was anteiso C15:0 (75%). Strain PNP1T grew optimally at 27°C, at pH 8-8.5, at salinities 3% (w/v) NaCl, yet exhibited a substantial halotolerance with growth occurring at salinities up to 17% (w/v) NaCl. In addition to para-nitrophenol, a range of sugars, short chain fatty acids and alcohols served as electron donors for growth. The DNA G + C mol% was 68%. The genotypic and phenotypic properties suggest that strain PNP1T represents a novel species of the actinobacterial genus Citricoccus for which the name Citricoccus nitrophenolicus is proposed. It is the first member of this genus that has been reported to hydrolyze and grow on para-nitrophenol. The type strain is PNP1T (=DSM 23311T = CCUG 59571T).

Keywords

Actinobacteria Taxonomy Para-nitrophenol degradation Xenobiotics 

Notes

Acknowledgments

The research was supported by a joint grant from Cheminova A/S, Central Denmark Region and The Aarhus University Research Foundation (AUFF). Thanks are due to Tove Wiegers for excellent technical assistance and to Inger Skov and Bo Breinbjerg for providing samples and information concerning the wastewater treatment plant at Cheminova A/S. Thanks are also due to J. P. Euzéby for providing the etymology of the species name. We are also indebted to the Editor and two anonymous reviewers for suggestions and comments that greatly improved the manuscript.

References

  1. Aelion CM, Swindoll CM, Pfaender F (1987) Adaptation to and biodegradation of xenobiotic compounds by microbial communities from a pristine aquifer. Appl Environ Microbiol 53:2212–2217PubMedGoogle Scholar
  2. Altenburger P, Kampfer P, Schumann P, Steiner R, Lubitz W, Busse H-J (2002a) Citricoccus muralis gen. nov., sp. nov., a novel actinobacterium isolated from a medieval wall painting. Int J Syst Evol Microbiol 52:2095–2100PubMedCrossRefGoogle Scholar
  3. Altenburger P, Kampfer P, Schumann P, Vybiral D, Lubitz W, Busse HJ (2002b) Georgenia muralis gen. nov., sp nov., a novel actinobacterium isolated from a medieval wall painting. Int J Syst Evol Microbiol 52:875–881PubMedCrossRefGoogle Scholar
  4. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  5. Boyd SA, Shelton DR, Berry D, Tiedje JM (1983) Anaerobic biodegradation of phenolic compounds in digested sludge. Appl Environ Microbiol 46:50–54PubMedGoogle Scholar
  6. Brucker MC (1986) Gram staining—a useful laboratory technique. J Nurse-Midwifery 31:156–158PubMedCrossRefGoogle Scholar
  7. Chauhan A, Chakraborti AK, Jain RK (2000) Plasmid-encoded degradation of p-nitrophenol and 4-nitrocatechol by Arthrobacter protophormiae. Biochem Biophysic Res Commun 270:733–740CrossRefGoogle Scholar
  8. Chun J, Lee J-H, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261PubMedCrossRefGoogle Scholar
  9. Coutu C, Martineau G, Guy C, Samson R (2003) Characterization of an organic filter medium for the biofiltration treatment of air contaminated with 1, 2-dichlorobenzene. J Chem Tech Biotechnol 78:907–917CrossRefGoogle Scholar
  10. Donlon BA, Razo-Flores E, Lettinga G, Field JA (1996) Continuous detoxification, transformation, and degradation of nitrophenols in upflow anaerobic sludge blanket (UASB) reactors. Biotechnol Bioeng 51:439–449PubMedCrossRefGoogle Scholar
  11. Errampalli D, Tresse O, Lee H, Trevors JT (1999) Bacterial survival and mineralization of p-nitrophenol in soil by green fluorescent protein-marked Moraxella sp. G21 encapsulated cells. FEMS Microbiol Ecol 30:229–236PubMedCrossRefGoogle Scholar
  12. Gemini VL, Gallego A, de Oliveira VM, Gomez CE, Manfio GP, Korol SE (2005) Biodegradation and detoxification of p-nitrophenol by Rhodococcus wratislaviensis. Int Biodet Biodegrad 55:103–108CrossRefGoogle Scholar
  13. Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis, 3rd edn. Wiley-VCH, Weinheim, Germany, pp 159–228CrossRefGoogle Scholar
  14. Ingvorsen K, Jørgensen BB (1984) Kinetics of sulfate uptake by freshwater and marine species of Desulfovibrio. Arch Mirobiol 139:61–66CrossRefGoogle Scholar
  15. Kadiyala V, Spain JC (1998) A two-component monooxygenase catalyzes both the hydroxylation of p-nitrophenol and the oxidative release of nitrite from 4-nitrocatechol in Bacillus sphaericus JS905. Appl Environ Microbiol 64:2479–2484PubMedGoogle Scholar
  16. Kalsch W, Knacker T, Danneberg G, Studinger G, Franke C (1999) Biodegradation of [14C]-4-nitrophenol in a sediment-water simulation test. Int Biodeter Biodegrad 44:65–74CrossRefGoogle Scholar
  17. Kitagawa W, Kimura N, Kamagata Y (2004) A novel p-nitrophenol degradation gene cluster from a Gram-positive bacterium, Rhodococcus opacus SAO101. J Bacteriol 186:4894–4902PubMedCrossRefGoogle Scholar
  18. Knudsen L, Kristensen GH, Jørgensen PE, Jepsen S-E (2000) Reduction of the content of organic micropollutants in digested sludge by a post-aeration process—a full-scale demonstration. Water Sci Technol 42:111–118Google Scholar
  19. Kulkarni M, Chaudhari A (2006) Biodegradation of p-nitrophenol by P. putida. Bioresource Technol 97:982–988CrossRefGoogle Scholar
  20. Labana S, Pandey G, Paul D, Sharma NK, Basu A, Jain RK (2005) Pot and field studies on bioremediation of p-nitrophenol contaminated soil using Arthrobacter protophormiae RKJ1100. Environ Sci Technol 39:3330–3337PubMedCrossRefGoogle Scholar
  21. Leung KT, Moore M, Lee H, Trevors JT (2005) Effect of carbon starvation on p-nitrophenol degradation by a Moraxella strain in buffer and river water. FEMS Microbiol Ecol 51:237–245PubMedCrossRefGoogle Scholar
  22. Li WJ, Chen HH, Zhang YQ, Kim CJ, Park DJ, Lee JC, Xu LH, Jiang CL (2005) Citricoccus alkalitolerans sp nov., a novel actinobacterium isolated from a desert soil in Egypt. Int J Syst Evol Microbiol 55:87–90PubMedCrossRefGoogle Scholar
  23. Løkke H (1985) Degradation of 4-nitrophenol in two Danish soils. Environ Pollut Ser A 38:171–181CrossRefGoogle Scholar
  24. Löser C, Oubelli MA, Hertel T (1998) Growth kinetics of the 4-nitrophenol degrading strain Pseudomonas putida PNP1. Acta Biotechnol 18:29–41CrossRefGoogle Scholar
  25. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K-H (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371PubMedCrossRefGoogle Scholar
  26. Martínez-Luque M, Castillo F (1991) Inhibition of aconitase and fumarase by nitrogen compounds in Rhodobacter capsulatus. Arch Microbiol 155:149–152CrossRefGoogle Scholar
  27. Meng F-X, Yang X-C, Yu P-S, Pan JM, Wang C-S, Xu X-W, Wu M (2010) Citricoccus zhacaiensis sp. nov., isolated from a bioreactor for saline wastewater treatment. Int J Syst Evol Microbiol 60:495–499PubMedCrossRefGoogle Scholar
  28. Mogensen GL, Kjeldsen KU, Ingvorsen K (2005) Desulfovibrio aerotolerans sp. nov., an oxygen tolerant sulfate-reducing bacterium isolated from activated sludge. Anaerobe 11:339–349PubMedCrossRefGoogle Scholar
  29. Moreno-Vivián C, Cárdenas J, Blasco R, Castillo F (1986) In vivo short-term inhibition of nitrogenase by nitrate in Rhodopseudomonas capsulata E1F1. FEMS Microbiol Lett 34:105–109Google Scholar
  30. PAN (2008) The pesticide action network (PAN) pesticide database: www.pesticideinfo.org
  31. Perry LL, Zylstra GJ (2007) Cloning of a gene cluster involved in the catabolism of p-nitrophenol by Arthrobacter sp. strain JS443 and characterization of the p-nitrophenol monooxygenase. J Bacteriol 189:7563–7572PubMedCrossRefGoogle Scholar
  32. Powers WM (1995) Efficacy of the Ryu nonstaining KOH technique for rapidly determining Gram reactions of food-borne and waterborne bacteria and yeasts. Appl Environ Microbiol 61:3756–3758PubMedGoogle Scholar
  33. Prakash D, Chauhan A, Jain RK (1996) Plasmid-encoded degradation of p-nitrophenol by Pseudomonas cepacia. Biochem Biophys Res Commun 224:375–381PubMedCrossRefGoogle Scholar
  34. Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO (2007) Silva a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acid Res 35:7188–7196PubMedCrossRefGoogle Scholar
  35. Qiu X-H, Bai W-Q, Zhong Q-Z, Li M, He F-Q, Li B-T (2006) Isolation and characterization of a bacterial strain of the genus Orchrobactrum with methyl parathion mineralizing activity. J Appl Microbiol 101:986–994PubMedCrossRefGoogle Scholar
  36. Roldan MD, Blasco R, Caballero FJ, Castillo F (1998) Degradation of p-nitrophenol by the phototrophic bacterium Rhodobacter capsulatus. Arch Microbiol 160:36–42Google Scholar
  37. Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedCrossRefGoogle Scholar
  38. Schäfer J, Martin K, Kämpfer P (2010) Citricoccus parietis sp. nov., isolated from a mould-colonized wall and emended description of Citricoccus alkalitolerans Li et al. 2005. Int J Syst Evol Microbiol 60:271–274PubMedCrossRefGoogle Scholar
  39. Singh B, Walker A (2006) Microbial degradation of organophosphorus compopunds. FEMS Microbiol Rev 30:428–471PubMedCrossRefGoogle Scholar
  40. Smibert RM, Krieg NR (1981) Phenotypic characterization. In: Gerhardt P (ed) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC, pp 607–654Google Scholar
  41. Spain JC (1995) Biodegradation of nitroaromatic compounds. Annu Rev Microbiol 49:523–555PubMedCrossRefGoogle Scholar
  42. Spain JC, Gibson DT (1991) Pathway for biodegradation of p-nitrophenol in a Moraxella sp. Appl Environ Microbiol 57:812–819PubMedGoogle Scholar
  43. Spain JC, Pritchard PH, Bourquin AW (1980) Effects of adaptation on biodegradation rates in sediment/water cores from estuarine and freshwater environments. Appl Environ Microbiol 40:726–734PubMedGoogle Scholar
  44. Spain JC, van Veld PA, Monti CA, Pritchard PH, Cripe CR (1984) Comparison of p-nitrophenol biodegradation in field and laboratory test systems. Appl Environ Microbiol 48:944–950PubMedGoogle Scholar
  45. Stanbury PF, Whitaker A, Hall SJ (1995) Principles of fermentation technology, 2nd edn. Pergamon, Oxford, p 96Google Scholar
  46. Tomei MC, Annesini MC, Luberti R, Cento G, Senia A (2003) Kinetics of 4-nitrophenol biodegradation in a sequencing batch reactor. Water Res 37:3803–3814PubMedCrossRefGoogle Scholar
  47. Trapido M, Kallas J (2000) Advanced oxidation processes for the degradation and detoxification of 4-nitrophenol. Environ Technol 21:799–808CrossRefGoogle Scholar
  48. Uberoi V, Bhattacharya SK (1997) Toxicity and degradability of nitrophenols in anaerobic systems. Water Environ Res 69:146–156CrossRefGoogle Scholar
  49. Volskay VT, Grady CPL (1990) Respiration inhibition kinetic analysis. Wat Res 24:863–874CrossRefGoogle Scholar
  50. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematic. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Marie Bank Nielsen
    • 1
  • Kasper Urup Kjeldsen
    • 2
  • Kjeld Ingvorsen
    • 1
    Email author
  1. 1.Department of Biological Sciences, MicrobiologyAarhus UniversityAarhus CDenmark
  2. 2.Center for Geomicrobiology, Department of Biological SciencesAarhus UniversityAarhus CDenmark

Personalised recommendations