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The Impact of Nitrite on Aerobic Growth of Paracoccus Denitrificans PD1222

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The Impact of Nitrite on Aerobic Growth of Paracoccus Denitrificans PD1222 Katherine Hartop | January 2014 The Impact of Nitrite on Aerobic Growth of Paracoccus denitrificans PD1222 Submitted for approval by Katherine Rachel Hartop BSc (Hons) For the qualification of Doctor of Philosophy University of East Anglia School of Biological Sciences January 2014 This copy of the thesis has been supplied on conditions that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. i Katherine Hartop | January 2014 Acknowledgments Utmost thanks go to my supervisors Professor David Richardson, Dr Andy Gates and Dr Tom Clarke for their continual support and boundless knowledge. I am also delighted to have been supported by the funding of the University of East Anglia for the length of my doctorial research. Thank you to the Richardson laboratory as well as those I have encountered and had the honour of collaborating with from the School of Biological Sciences. Thank you to Georgios Giannopoulos for your contribution to my research and support during the writing of this thesis. Thanks to my friends for their patience, care and editorial input. Deepest thanks to Dr Rosa María Martínez-Espinosa and Dr Gary Rowley for examining me and my research. This work is dedicated to my parents, Keith and Gill, and my family. ii Katherine Hartop | January 2014 Abstract The effect of nitrite stress induced in Paracoccus denitrificans PD1222 was examined using additions of sodium nitrite to an aerobic bacterial culture. Nitrite generates a strong stress response in P. denitrificans, causing growth inhibition. This is dependent on both the concentration of nitrite present and the pH. The pH dependent effect of nitrite growth inhibition is likely a result of nitrite and free nitrous acid (FNA; pKa = 3.16) and subsequent reactive nitrogen oxides, generated from the intracellular passage of FNA into P. denitrificans. A flavohemoglobin (fhb; Pd1689) and its associated NsrR family, transcriptional regulator (Pd1690), were transcribed above a ≥2 fold expression filter (p ≤ 0.05) at 95% significance in qRT-PCR and a type II microarray transcriptional analysis at 12.5 mM nitrite in batch culture. Additionally, >25 fold expression of the flavohemoglobin was confirmed by qRT-PCR in continuous culture with nitrite. A deletion mutant determined fhb to be involved in conveying nitrite resistance at high nitrite concentrations and is linked to a stimulation of biomass generated by the presence of nitrite. The cytochrome ba3 oxidase was found to be associated with nitrite in transcriptional analysis, suggesting the uncoupling of the protonmotive force caused by the transport of FNA across the membrane, and subsequent dissociation in the cytoplasm were reduced by a method of counterbalance. No nitrate accumulation was seen and nitrous oxide levels were above that observed for atmospheric background levels. The microarray analysis was used to confirm that in batch growth at 12.5 mM nitrite addition, P. denitrificans shows an overall stress response associated with protein, DNA and lipid repair, with the addition of fhb detoxification and action of the cytochrome ba3 oxidase. It is therefore suggested that nitrite presents a pH- dependent stress response in P. denitrificans, likely due to the production of associated reactive nitrogen species such as NO from the internalisation of FNA and the uncoupling of the protonmotive force. iii Katherine Hartop | January 2014 1 Introduction Contents 1 Introduction ............................................................................................................ 1 1.1 List of figures .................................................................................................. 2 1.2 The Nitrogen Cycle .......................................................................................... 3 1.2.1 Nitrogen fixation....................................................................................... 4 1.2.2 Ammonia immobilisation and ammonification............................................ 6 1.2.3 Nitrification.............................................................................................. 7 1.2.4 Nitrogen assimilation ................................................................................ 8 1.2.5 Anaerobic ammonium oxidation (anammox) .............................................. 8 1.2.6 Denitrification ........................................................................................ 10 1.3 The reactive nature of nitrogen oxides ............................................................. 11 1.3.1 Nitric oxide and its breakdown products ................................................... 12 1.3.2 Peroxynitrite and the generation of nitric oxide ......................................... 13 1.3.3 Wastewater and the environmental impact of nitrogen oxides .................... 14 1.3.4 Recent increases in atmospheric nitrous oxide levels ................................. 15 1.4 P. denitrificans as a model denitrifying microorganism.................................... 17 1.4.1 Nitrate reduction by the cytoplasmic nitrate reductase (NAR) in P. denitrificans .......................................................................................................... 20 1.4.2 Nitrate reduction by the periplasmic nitrate reductase (NAP) ..................... 22 1.4.3 Nitrate reduction in the bacterial assimilatory pathway (NAS) ................... 26 1.4.4 The nitrite, nitric oxide and nitrous oxide reductases ................................. 27 1.5 Aims ............................................................................................................. 30 1.6 References ..................................................................................................... 31 1 Katherine Hartop | January 2014 1.1 List of figures Figure 1.1: Schematic illustrating the nitrogen cycle, showing the processes of nitrogen fixation. The atmosphere nitrogen (N2) (with an oxidation state of 0) is converted to + ammonium (NH4 ; -3), which can be either be immobilised into the cellular structure of - organisms, or oxidised via the hydroxylamine ion (NH2OH; -1) to nitrite (NO2 ; +3) and - nitrate (NO3 ; +5) during nitrification. Ammonification or mineralisation of cellular bound - organic nitrogen reintroduces nitrogen in the form of ammonia. NO3 can then be reduced to - NO2 , nitric oxide (NO; +2), nitrous oxide (N2O; +1) and returned to N2 by denitrification. Additionally, anommox (anaerobic ammonium oxidation) also returns nitrogen from + - NH4 and NO2 to N2. Heterotrophic nitrification oxidises NH2OH to form N2O and is a route to N2O emissions from the nitrification pathway. Finally the three processes of respiration, - - dissimilation and assimilation all contribute to convert NO3 to NO2 . (Adapted from Richardson (2001) and Nature Education © 2010.) ........................................................... 5 Figure 1.2. A: Haber Bosch processing for the industrialised production of nitrate fertiliser. The Haber process combines nitrogen from the air with hydrogen, derived mainly from natural gas (methane), into ammonia. The reaction is reversible and the production of ammonia is exothermic. B: Impact of manure production, fertiliser production on atmospheric N2O production per year (sources: The European Environment Agency (EEA) and Intergovernmental Panel on Climate Change (IPCC))................................................ 16 Figure 1.3: Respiratory chain for P. denitrificans. The movement of electrons is shown by orange arrows. Electron donors such as hydrogenases, the NADH-UQ oxidoreductase and succinate dehydrogenase provide electrons to the Ubiquinol Pool (Q-Pool) generating the formation of Ubiquinol and pumping protons into the periplasm. These electrons are then passed to the nitrate reductases and ubiquinol cytochrome c oxidoreductase, which in turn passes electrons to the cytochrome c550 / pseudoazurin and cytochrome c552. Finally electrons pass to the cbb3 and aa3 oxidase, nitrite reductase, nitric oxide reductase, nitrous oxide reductase and cytochrome c peroxidase. ......................................................................... 19 Figure 1.4: Oxidative phosphorylation pathway featuring the NADH-UQ oxidoreductase (complex I), succinate dehydrogenase (complex II), cytochrome bc1 complex (complex III), cytochrome aa3 oxidase (complex IV) and ATP synthase. ............................................... 21 Figure 1.5: A schematic for metabolism of fatty acids in P. denitrificans and up-regulation of the periplasmic nitrate reductase (NapAB). A: β-Oxidation pathway showing metabolism of butyrate to form Acetyl Co-A. Reducing equivalents NADH and FADH2 are produced by β-Oxidation and enter the Q-Pool reduce ubiquinone to ubiquinol. B: Activation of the 2 Katherine Hartop | January 2014 NapAB complex accepting electrons taken from the Q-Pool via NapC to reduce nitrate to nitrite, converting the excess ubiquinol to ubiquinone. The Q-Pool is rebalanced. ............. 24 Figure 1.6: Enzymes available under aerobic growth conditions in P. denitrificans. Featuring nitrate reduction by NapABC; generation of free nitrous acid passing across the periplasmic membrane; decomposition and disproportionation of nitrogenous species in the cytoplasm; detoxification of nitric oxide (NO) by NorBC; generation of ammonia by NasC and NasBG; ammonia assimilation
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