J. Bacteriol., Aug 1996, 4367-4374, Vol 178, No. 15
Copyright © 1996, American Society for Microbiology

Dynamics of denitrification activity of Paracoccus denitrificans in continuous culture during aerobic-anaerobic changes

B Baumann, M Snozzi, AJ Zehnder and JR Van Der Meer
Swiss Federal Institute of Environmental Science and Technology, Dubendorf, Switzerland.

Induction and repression of denitrification activity were studied in a continuous culture of Paracoccus denitrificans during changes from aerobic to anaerobic growth conditions and vice versa. The denitrification activity of the cells was monitored by measuring the formation of denitrification products (nitrite, nitric oxide, nitrous oxide, and dinitrogen), individual mRNA levels for the nitrate, nitrite, and nitrous oxide reductases, and the concentration of the nitrite reductase enzyme with polyclonal antibodies against the cd1- type nitrite reductase. On a change from aerobic to anaerobic respiration, the culture entered an unstable transition phase during which the denitrification pathway became induced. The onset of this phase was formed by a 15- to 45-fold increase of the mRNA levels for the individual denitrification enzymes. All mRNAs accumulated during a short period, after which their overall concentration declined to reach a stable value slightly higher than that observed under aerobic steady- state conditions. Interestingly, the first mRNAs to be formed were those for nitrate and nitrous oxide reductase. The nitrite reductase mRNA appeared significantly later, suggesting different modes of regulation for the three genes. Unlike the mRNA levels, the level of the nitrite reductase protein increased slowly during the anaerobic period, reaching a stable value about 30 h after the switch. All denitrification intermediates could be observed transiently, but when the new anaerobic steady state was reached, dinitrogen was the main product. When the anaerobic cultures were switched back to aerobic respiration, denitrification of the cells stopped at once, although sufficient nitrite reductase was still present. We could observe that the mRNA levels for the individual denitrification enzymes decreased slightly to their aerobic, uninduced levels. The nitrite reductase protein was not actively degraded during the aerobic period.

This article has been cited by other articles:

• Hunt, P. G., Matheny, T. A., Ro, K. S. (2007). Nitrous Oxide Accumulation in Soils from Riparian Buffers of a Coastal Plain Watershed Carbon/Nitrogen Ratio Control. J. Environ. Qual. 36: 1368-1376 [Abstract] [Full Text]  
• Beller, H. R., Letain, T. E., Chakicherla, A., Kane, S. R., Legler, T. C., Coleman, M. A. (2006). Whole-Genome Transcriptional Analysis of Chemolithoautotrophic Thiosulfate Oxidation by Thiobacillus denitrificans under Aerobic versus Denitrifying Conditions.. J. Bacteriol. 188: 7005-7015 [Abstract] [Full Text]  
• Lee, Y.-Y., Shearer, N., Spiro, S. (2006). Transcription factor NNR from Paracoccus denitrificans is a sensor of both nitric oxide and oxygen: isolation of nnr* alleles encoding effector-independent proteins and evidence for a haem-based sensing mechanism.. Microbiology 152: 1461-1470 [Abstract] [Full Text]  
• Gaillard, M., Vallaeys, T., Vorholter, F. J., Minoia, M., Werlen, C., Sentchilo, V., Puhler, A., van der Meer, J. R. (2006). The clc Element of Pseudomonas sp. Strain B13, a Genomic Island with Various Catabolic Properties.. J. Bacteriol. 188: 1999-2013 [Abstract] [Full Text]  
• Horn, M. A., Mertel, R., Gehre, M., Kastner, M., Drake, H. L. (2006). In Vivo Emission of Dinitrogen by Earthworms via Denitrifying Bacteria in the Gut. Appl. Environ. Microbiol. 72: 1013-1018 [Abstract] [Full Text]  
• Kuypers, M. M. M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B. M., Amann, R., Jorgensen, B. B., Jetten, M. S. M. (2005). From The Cover: Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102: 6478-6483 [Abstract] [Full Text]  
• Suar, M., van der Meer, J. R., Lawlor, K., Holliger, C., Lal, R. (2004). Dynamics of Multiple lin Gene Expression in Sphingomonas paucimobilis B90A in Response to Different Hexachlorocyclohexane Isomers. Appl. Environ. Microbiol. 70: 6650-6656 [Abstract] [Full Text]  
• Mazoch, J., Kunak, M., Kucera, I., van Spanning, R. J. M. (2003). Fine-tuned regulation by oxygen and nitric oxide of the activity of a semi-synthetic FNR-dependent promoter and expression of denitrification enzymes in Paracoccus denitrificans. Microbiology 149: 3405-3412 [Abstract] [Full Text]  
• Pearson, I. V., Page, M. D., van Spanning, R. J. M., Ferguson, S. J. (2003). A Mutant of Paracoccus denitrificans with Disrupted Genes Coding for Cytochrome c550 and Pseudoazurin Establishes These Two Proteins as the In Vivo Electron Donors to Cytochrome cd1 Nitrite Reductase. J. Bacteriol. 185: 6308-6315 [Abstract] [Full Text]  
• Sentchilo, V., Ravatn, R., Werlen, C., Zehnder, A. J. B., van der Meer, J. R. (2003). Unusual Integrase Gene Expression on the clc Genomic Island in Pseudomonas sp. Strain B13. J. Bacteriol. 185: 4530-4538 [Abstract] [Full Text]  
• Takaya, N., Catalan-Sakairi, M. A. B., Sakaguchi, Y., Kato, I., Zhou, Z., Shoun, H. (2003). Aerobic Denitrifying Bacteria That Produce Low Levels of Nitrous Oxide. Appl. Environ. Microbiol. 69: 3152-3157 [Abstract] [Full Text]  
• Ihssen, J., Horn, M. A., Matthies, C., Gossner, A., Schramm, A., Drake, H. L. (2003). N2O-Producing Microorganisms in the Gut of the Earthworm Aporrectodea caliginosa Are Indicative of Ingested Soil Bacteria. Appl. Environ. Microbiol. 69: 1655-1661 [Abstract] [Full Text]  
• Horn, M. A., Schramm, A., Drake, H. L. (2003). The Earthworm Gut: an Ideal Habitat for Ingested N2O-Producing Microorganisms. Appl. Environ. Microbiol. 69: 1662-1669 [Abstract] [Full Text]  
• Taroncher-Oldenburg, G., Griner, E. M., Francis, C. A., Ward, B. B. (2003). Oligonucleotide Microarray for the Study of Functional Gene Diversity in the Nitrogen Cycle in the Environment. Appl. Environ. Microbiol. 69: 1159-1171 [Abstract] [Full Text]  
• Nogales, B., Timmis, K. N., Nedwell, D. B., Osborn, A. M. (2002). Detection and Diversity of Expressed Denitrification Genes in Estuarine Sediments after Reverse Transcription-PCR Amplification from mRNA. Appl. Environ. Microbiol. 68: 5017-5025 [Abstract] [Full Text]  
• Laratta, W. P., Choi, P. S., Tosques, I. E., Shapleigh, J. P. (2002). Involvement of the PrrB/PrrA Two-Component System in Nitrite Respiration in Rhodobacter sphaeroides 2.4.3: Evidence for Transcriptional Regulation. J. Bacteriol. 184: 3521-3529 [Abstract] [Full Text]  
• Sun, J., Smets, I., Bernaerts, K., Van Impe, J., Vanderleyden, J., Marchal, K. (2001). Quantitative Analysis of Bacterial Gene Expression by Using the gusA Reporter Gene System. Appl. Environ. Microbiol. 67: 3350-3357 [Abstract] [Full Text]  
• Jaspers, M. C. M., Schmid, A., Sturme, M. H. J., Goslings, D. A. M., Kohler, H.-P. E., Roelof van der Meer, J. (2001). Transcriptional Organization and Dynamic Expression of the hbpCAD Genes, Which Encode the First Three Enzymes for 2-Hydroxybiphenyl Degradation in Pseudomonas azelaica HBP1. J. Bacteriol. 183: 270-279 [Abstract] [Full Text]  
• Saito, A., Ishizaka, M., Francisco, P. B. Jr, Fujii, T., Miyashita, K. (2000). Transcriptional co-regulation of five chitinase genes scattered on the Streptomyces coelicolor A3(2) chromosome. Microbiology 146: 2937-2946 [Abstract] [Full Text]  
• Laemmli, C. M., Leveau, J. H. J., Zehnder, A. J. B., van der Meer, J. R. (2000). Characterization of a Second tfd Gene Cluster for Chlorophenol and Chlorocatechol Metabolism on Plasmid pJP4 in Ralstonia eutropha JMP134(pJP4). J. Bacteriol. 182: 4165-4172 [Abstract] [Full Text]  
• Uemoto, H., Saiki, H. (2000). Distribution of Nitrosomonas europaea and Paracoccus denitrificans Immobilized in Tubular Polymeric Gel for Nitrogen Removal. Appl. Environ. Microbiol. 66: 816-819 [Abstract] [Full Text]  
• Murray, R. E., Knowles, R. (1999). Chloramphenicol Inhibition of Denitrifying Enzyme Activity in Two Agricultural Soils. Appl. Environ. Microbiol. 65: 3487-3492 [Abstract] [Full Text]  
• Härtig, E., Zumft, W. G. (1999). Kinetics of nirS Expression (Cytochrome cd1 Nitrite Reductase) in Pseudomonas stutzeri during the Transition from Aerobic Respiration to Denitrification: Evidence for a Denitrification-Specific Nitrate- and Nitrite-Responsive Regulatory System. J. Bacteriol. 181: 161-166 [Abstract] [Full Text]