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Chapter 14 : Periplasmic Nitrate Reduction

Author: Jeff A. Cole1
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Affiliations: 1: School of Biosciences, University of Birmingham, Birmingham B15 2TT, United Kingdom
Content Type: Monograph
Publication Year: 2007

Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology

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Abstract:

Before 1980, just two types of bacterial nitrate reductase were widely recognized: these were the soluble, cytoplasmic nitrate reductases involved in nitrate assimilation and the membrane-associated respiratory nitrate reductases. It rapidly became apparent that, in contrast to the more conserved components of the membrane-associated respiratory nitrate reductase encoded by the narGHJI operons, there were at least five levels of diversity among the periplasmic nitrate reductases: their distribution among bacteria of different physiological types; their regulation; their physiological roles; their components; and their genetic context. This chapter reviews each of these aspects followed by a summary of recent developments, including the realization by Richardson and his colleagues that there is a fourth type of nitrate reductase, a membrane-associated group with catalytic sites located in the periplasm, which might explain how the diversity of the Nap enzymes has evolved. Twelve different types of polypeptide are encoded by the various nap clusters, but only two of them, and , have so far always been found together. Further support for the ideas of Richardson and Jepson comes from the nap gene cluster in , which includes a gene encoding a small tetraheme c-type cytochrome homologous to NapM. Given that the sulfate:sulfite redox couple is strongly electronegative compared with the nitrate:nitrite couple, it would be fascinating to determine whether nitrate reduction by is repressed by sulfate.

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14

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Integral Membrane Proteins
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Nitrate Reduction
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Nitrate Reductase
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Periplasmic Nitrate Reduction
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Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
/content/10.1128/9781555815806.ch14.ch14fig01
FIGURE 1
Electron transfer to NapA in different bacteria.
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10.1128/9781555815806/f0253-01.gif
Image of FIGURE 1
FIGURE 1

Electron transfer to NapA in different bacteria.

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
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FIGURE 2
Evolution of cytochrome -linked periplasmic nitrate reductases.
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Image of FIGURE 2
FIGURE 2

Evolution of cytochrome -linked periplasmic nitrate reductases.

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
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References

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1. Alef, K., and, J. H. Klemme. 1977. Characterization of a soluble NADH-independent nitrate reductase from the photosynthetic bacterium Rhodopseudomonas capsulata. Z. Naturforsch. 32: 954– 956.
2. Arnoux, P.,, M. Sabaty,, J. Alric,, B. Frangioni,, B. Guigliarelli,, J. M. Adriano, and, D. Pignol. 2003. Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase. Nat. Struct. Biol. 10: 928– 934.
3. Bedzyk, L.,, T. Wang, and, R. W. Ye. 1999. The periplasmic nitrate reductase in Pseudomonas sp. strain G-179 catalyzes the first step of denitrification. J. Bacteriol. 181: 2802– 2806.
4. Berks, B. C.,, D. J. Richardson,, A. Reilly,, A. C. Willis, and, S. J. Ferguson. 1995. The napEDABC gene cluster encoding the periplasmic nitrate reductase system of Thiosphaera pantotropha. Biochem.J 309: 983– 992.
5. Bertero, M. G.,, R. A. Rothery,, M. Palak,, C. Hou,, D. Lim,, F. Blasco,, J. H. Weiner, and, N. C. Strynadka. 2003. Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat. Struct. Biol. 10: 681– 687.
6. Brige, A.,, D. Leys,, T. E. Meyer,, M. A. Cusanovich, and, J. J. Van Beeumen. 2002. The 1.25 A resolution structure of the diheme NapB subunit of soluble nitrate reductase reveals a novel cytochrome c fold with a stacked heme arrangement. Biochemistry 41: 4827– 4836.
7. Brondijk, T. H.,, D. Fiegen,, D. J. Richardson, and, J. A. Cole. 2002. Roles of NapF, NapG and NapH, subunits of the Escherichia coli periplasmic nitrate reductase, in ubiquinol oxidation. Mol. Microbiol. 44: 245– 255.
8. Brondijk, T. H.,, A. Nilavongse,, N. Filenko,, D. J. Richardson, and, J. A. Cole. 2004. The NapGH components of the periplasmic nitrate reductase of Escherichia coli K-12: location, topology, and physiological roles in quinol oxidation and redox balancing. Biochem. J. 379: 47– 55.
9. Bursakov, S.,, M.-Y. Liu,, W. J. Payne,, J. LeGall,, I. Moura, and, J. J. G. Moura. 1995. Isolation and preliminary characterisation of a soluble nitrate reductase from the sulphate reducing organism Desulfovibrio desulfuricansATCC 27774. Anaerobe 1: 55– 60.
10. Butler, C. S.,, J. M. Charnock,, B. Bennett,, H. J. Sears,, A. J. Reilly,, S. J. Ferguson,, C. D. Garner,, D. J. Lowe,, A. D. Thomson,, B. C. Berks, and, D. J. Richardson. 1999. Models for molybdenum coordination during the catalytic cycle of periplasmic nitrate reductase from Paracoccus denitrificans derived from EPR and EXAFS spectroscopy. Biochemistry 38: 9000– 9012.
11. Damborsky, J., 1999. Tetrachloroethene-dehalogenating bacteria. Folia Microbiol. (Praha) 44: 247– 262.
12. Dias, J. M.,, M. E. Than,, A. Humm,, R. Huber,, G. P. Bourenkov,, H. D. Bartunik,, S. Bursakov,, J. Calvete,, J. Caldeira,, C. Carneiro,, J. J. Moura,, I. Moura, and, M. J. Romao. 1999. Crystal structure of the first dissimilatory nitrate reductase at 1.9 A solved by MAD methods. Structure 7: 65– 79.
13. Ellington, M. J.,, D. J. Richardson, and, S. J. Ferguson. 2003. .Rhodobacter capsulatus gains a competitive advantage from respiratory nitrate reduction during light-dark transitions. Microbiology 149: 941– 948.
14. Grove, J.,, S. Tanapongpipat,, G. Thomas,, L. Griffiths,, H. Crooke, and, J. Cole. 1996. Escherichia coli K-12 genes essential for the synthesis of c-type cytochromes and a third nitrate reductase located in the periplasm. Mol. Microbiol. 19: 467– 481.
15. Haveman, S. A.,, E. A. Greene,, C. P. Stillwell,, J. K. Voordouw, and, G. Voordouw. 2004. Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J. Bacteriol. 186: 7944– 7950.
16. Hettmann, T.,, R. A. Siddiqui,, C. Frey,, T. Santos Silva,, M. J. Romao, and, D. Diekmann. 2004. Mutagenesis study on amino acids around the molybdenum centre of the periplasmic nitrate reductase from Ralstonia eutropha. Biochem. Biophys. Res. Commun. 320: 1211– 1219.
17. Jepson, B. N.,, L. J. Anderson,, L. M. Rubio,, C. J. Taylor,, C. S. Butler,, E. Flores,, A. Herrero,, J. N. Butt, and, D. J. Richardson. 2004. Tuning a nitrate reductase for function. The first spectropotentiometric characterization of a bacterial assimilatory nitrate reductase reveals novel redox properties. J. Biol. Chem. 31: 32212– 32218.
18. Jepson, B. J. N.,, A. Marietou,, S. Mohan,, J. A. Cole,, C. S. Butler, and, D. J. Richardson. 2006. Evolution of the soluble nitrate reductase: defining the monomeric periplasmic nitrate reductase subgroup. Biochem. Soc. Trans. 34: 122– 126.
19. Jormakka, M.,, D. Richardson,, B. Byrne, and, S. Iwata. 2004. Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure 12: 95– 104.
20. Marietou, A.,, D. Richardson,, J. Cole, and, S. Mohan. 2005. Nitrate reduction by Desulfovibrio desulfuricans: a periplasmic nitrate reductase that lacks NapB, but includes a unique tetraheme c-type cytochrome, NapM. FEMS Microbiol Lett. 248: 217– 225.
21. Myers, C. R., and, J. M. Myers. 1997. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MKR-1. J. Bacteriol. 179: 1143– 1152.
22. Olmo-Mira, M. F.,, M. Gavira,, D. J. Richardson,, F. Castillo,, C. Moreno-Vivian, and, M. D. Roldan. 2004. NapF is a cytoplasmic iron-sulfur protein required for Fe-S cluster assembly in the periplasmic nitrate reductase. J. Biol. Chem. 26: 49727– 49735.
23. Palmer, T.,, C. L. Santini,, C. Iobbi-Nivol.,, D. J. Eaves,, D. H. Boxer, and, G. Giordano. 1996. Involvement of the narJ and mob gene products in distinct steps in the biosynthesis of the molybdoenzyme nitrate reductase in Escherichia coli. Mol. Microbiol. 20: 875– 884.
24. Potter, L.,, H. Angove,, D. Richardson, and, J. Cole. 2001. Nitrate reduction in the periplasm of Gramnegative bacteria. Adv. Microb. Physiol. 45: 51– 112.
25. Potter, L.,, P. Millington,, G. Thomas, and, J. Cole. 1999. Competition between Escherichia coli strains expressing either a periplasmic or a membranebound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth? Biochem. J. 344: 77– 84.
26. Potter, L. C., and, J. A. Cole. 1999. Essential roles for the products of the napABCD genes, but not napFGH, in periplasmic nitrate reduction by Escherichia coli K-12. Biochem. J. 344: 69– 76.
27. Rainey, F. A.,, D. P. Kelly,, E. Stackebrandt,, J. Burhardt,, A. Hiraishi,, Y. Katayama, and, A. P. Wood. 1999. A re-evaluation of the taxonomy of Paracoccus denitrificans and a proposal for the combination Paracoccus pantotrophus comb. nov. Int. J. Syst. Bacteriol. 49: 645– 651.
28. Reyes, F.,, M. Gavira,, F. Castillo, and, C. Moreno Vivian. 1998. Periplasmic nitrate reducing system of the phototrophic bacterium Rhodobacter sphaeroides DSM 158: transcriptional and mutational analysis of the napKEFDABC gene cluster. Biochem. J. 331: 897– 904.
29. Reyes, F.,, M. D. Roldan,, W. Klipp,, F. Castillo, and, C. Moreno-Vivian. 1996. Isolation of periplasmic nitrate reductase genes from Rhodobacter sphaeroides DSM 158: structural and functional differences among prokaryotic nitrate reductases. Mol. Microbiol. 19: 1307– 1318.
30. Richardson, D. J.,, A. G. McEwan,, M. D. Page,, J. B. Jackson, and, S. J. Ferguson. 1990. The identification of cytochromes involved in the transfer of electrons to the periplasmic NO 3¯ reductase of Rhodobacter capsulatus and resolution of a soluble NO 3¯ -reductase-cytochrome-c 552 redox complex. Eur. J. Biochem. 194: 263– 270.
31. Robertson, L. A., and, J. G. Kuenen. 1984. Aerobic denitrification–old wine in new bottles? Antonie van Leeuwenhoek 50: 525– 544.
32. Roldan, M. D.,, H. J. Sears,, S. J. Ferguson,, M. R. Cheeseman,, A. J. Thomson,, B. C. Berks, and, D. J. Richardson. 1998. Spectroscopic characterisation of a novel tetra-heme c-type cytochrome widely implicated in bacterial electron transport. J. Biol. Chem. 273: 28785– 28790.
33. Sargent, F.,, B. C. Berks, and, T. Palmer. 2002. Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch. Microbiol. 178: 77– 84.
34. Sears, H. J.,, G. Sawers,, B. C. Berks,, S. J. Ferguson, and, D. J. Richardson. 2000. Control of periplasmic nitrate reductase gene expression (napEDABC) from Paracoccus pantotrophus in response to oxygen and carbon substrates. Microbiology 146: 2977– 2985.
35. Sears, H. J.,, S. Spiro, and, D. J. Richardson. 1997. Effect of aeration and carbon substrate on expresion of the periplasmic and membrane-bound nitrate reductases of Paracoccus denitrificans. Microbiology 143: 3765– 3774.
36. Seki-Chiba, S., and, M. Ishimoto. 1977. Studies on nitrate reductase of Clostridium perfringens. Purification, some properties, and effect of tungstate on its formation. J. iochem. (Tokyo) 82: 1663– 1671.
37. Siddiqui R. A.,, U. Warnecke-Eberz,, A. Hengsberger,, B. Schneider,, S. Kostka, and, B. Friedrich. 1993. Structure and function of a periplasmic nitrate reductase in Alcaligenes eutrophus H16. J. Bacteriol. 175: 5867– 5876.
38. Simon, J.,, M. Sanger,, S. C. Schuster, and, R. Gross. 2003. Electron transport to periplasmic nitrate reductase (NapA) of Wolinella succinogenese is independent of a NapC protein. Mol. Microbiol. 49: 69– 79.
39. Tempest, D. W.,, J. L. Meers, and, C. M. Brown. 1970. Synthesis of glutamate in Aerobacter aerogenes by a hitherto unknown route. Biochem. J. 117: 405– 407.
40. Thomas, G.,, L. Potter, and, J. Cole. 1999. The periplasmic nitrate reductase of Escherichia coli: a heterodimeric molybdoprotein with a doublearginine signal sequence and an unusual leader peptide cleavage site. FEMS Microbiol. Lett. 174: 167– 171.
41. Ueda, K.,, A. Yamashita,, J. Ishikawa,, T. O. Watsuji,, H. Ikeda,, M. Hattori, and, T. Beppu. 2004. Genome sequence of Symbiobacterium thermophilum, an uncultivatable bacterium that depends on microbial commensalisms. Nucleic Acids Res. 32: 4937– 4944.
42. Wang, H.,, C. P. Tseng, and, R. P. Gunsalus. 1999. The napF and narG nitrate reductase operons in Escherichia coli are differentially expressed in response to submicromolar concentrations of nitrate but not nitrite. J. Bacteriol. 181: 5303– 5308.
43. Wood, N. J.,, T. Alizadeh,, S. Bennett,, J. Pearce,, S. J. Ferguson, and, J. W. Moir. 2001. Maximal expression of membrane-bound nitrate reductase in Paracoccus is induced by nitrate via a third FNR-like regulator named NarR. J. Bacteriol. 183: 3606– 3613.

Tables

Periplasmic Nitrate Reduction
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Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
/content/10.1128/9781555815806.ch14.ch14tab01
TABLE 1
Various physiological roles of Nap in different bacteria
Generic image for table
TABLE 1

Various physiological roles of Nap in different bacteria

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
/content/10.1128/9781555815806.ch14.ch14tab02
TABLE 2
Why an strain expressing a periplasmic nitrate reductase outcompetes a strain expressing only nitrate reductase A during nitrate-limited anaerobic growth
Generic image for table
TABLE 2

Why an strain expressing a periplasmic nitrate reductase outcompetes a strain expressing only nitrate reductase A during nitrate-limited anaerobic growth

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
/content/10.1128/9781555815806.ch14.ch14tab03
TABLE 3
Polypeptides encoded by gene clusters in various bacteria
Generic image for table
TABLE 3

Polypeptides encoded by gene clusters in various bacteria

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14
/content/10.1128/9781555815806.ch14.ch14tab04
TABLE 4
Variety of combinations of genes in the clusters of different strains
Generic image for table
TABLE 4

Variety of combinations of genes in the clusters of different strains

Citation: Cole J. 2007. Periplasmic Nitrate Reduction, p 247-259. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch14

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