Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Tiso, Mauro ^a   Schechter, Alan N ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; LACTIC ACID; NITRATE; NITRIC OXIDE; NITRITE; OXYGEN; SODIUM NITRATE; NITRIC ACID DERIVATIVE;

ACIDIFICATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BIFIDOBACTERIUM LONGUM SUBSP. INFANTIS; BIOACCUMULATION; CHEMICAL ANALYSIS; CHEMICAL MODIFICATION; CHEMICAL REACTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; INTESTINE FLORA; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; MAMMAL; METABOLISM; MICROBIAL ACTIVITY; NITRATE METABOLISM; NITRIC OXIDE METABOLISM; NITRITE METABOLISM; NONHUMAN; PH; PHYSIOLOGY; TIME; ANALYSIS OF VARIANCE; BIFIDOBACTERIUM; HUMAN; LACTOBACILLUS; NITROGEN CYCLE;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; ENTEROBACTERIACEAE; ESCHERICHIA COLI; LACTOBACILLUS; LACTOBACILLUS PLANTARUM; MAMMALIA;

AMMONIA; ANALYSIS OF VARIANCE; BIFIDOBACTERIUM; ESCHERICHIA COLI; GASTROINTESTINAL MICROBIOME; HUMANS; LACTIC ACID; LACTOBACILLUS; NITRATES; NITRIC OXIDE; NITRITES; NITROGEN CYCLE; OXYGEN;

EID: 84925605686     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119712     Document Type: Article

References (57)

1. Ignarro LJ. Nitric Oxide: Biology and Pathobiology. San Diego, CA: Academic Press; 2000.
2. Lundberg JM, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov. 2008 Feb; 7(2):156-67. doi: 10.1038/nrd2466 PMID: 18167491
3. Nathan S Bryan JL. Nitrite and Nitrate in Human Health and Disease (Nutrition and Health). 2013 Jul 17;:1-330.
4. Lundberg JM, Weitzberg E, Cole J, Benjamin N. Nitrate, bacteria and human health. Nat Rev Micro. 2004 Jul 1; 2(7):593-602. PMID: 15197394
5. Van Faassen EE, Bahrami S, Feelisch M, Hogg N, Kelm M, Kim-Shapiro DB, et al. Nitrite as regulator of hypoxic signaling in mammalian physiology. Med Res Rev. 2009 Sep; 29(5):683-741. doi: 10.1002/med.20151 PMID: 19219851
6. Castiglione N, Rinaldo S, Giardina G, Stelitano V, Cutruzzolà F. Nitrite and nitrite reductases: from molecular mechanisms to significance in human health and disease. Antioxidants & Redox Signaling. 2012 Aug 15; 17(4):684-716.
7. Tannenbaum SR, Fett D, Young VR, Land PD, Bruce WR. Nitrite and nitrate are formed by endogenous synthesis in the human intestine. Science. 1978 Jun 30; 200(4349):1487-9. PMID: 663630
8. Lidder S, Webb AJ. Vascular effects of dietary nitrate (as found in green leafy vegetables and beetroot) via the nitrate-nitrite-nitric oxide pathway. 2013 Mar; 75(3):677-96. doi: 10.1111/j.1365-2125.2012.04420.x PMID: 22882425
9. Govoni M, Jansson EA, Weitzberg E, Lundberg JM. The increase in plasma nitrite after a dietary nitrate load is markedly attenuated by an antibacterial mouthwash. Nitric Oxide. 2008 Dec; 19(4):333-7. doi: 10.1016/j.niox.2008.08.003 PMID: 18793740
10. Raat NJH, Noguchi AC, Liu VB, Raghavachari N, Liu D, Xu X, et al. Dietary nitrate and nitrite modulate blood and organ nitrite and the cellular ischemic stress response. Free Radical Biology and Medicine. 2009 Sep 1; 47(5):510-7. doi: 10.1016/j.freeradbiomed.2009.05.015 PMID: 19464364
11. Weitzberg E, Lundberg JM. Novel aspects of dietary nitrate and human health. Annu Rev Nutr. 2013; 33(1):129-59.
12. Bartholomew B, Hill MJ. The pharmacology of dietary nitrate and the origin of urinary nitrate. Food Chem Toxicol. 1984 Oct; 22(10):789-95. PMID: 6541617
13. Green LC, Tannenbaum SR, Goldman P. Nitrate synthesis in the germfree and conventional rat. Science. 1981 Apr 3; 212(4490):56-8. PMID: 6451927
14. Wagner DA, Schultz DS, Deen WM, Young VR, Tannenbaum SR. Metabolic Fate of an Oral Dose of 15N-labeled Nitrate in Humans: Effect of Diet Supplementation with Ascorbic Acid. Cancer Res. American Association for Cancer Research; 1983 Apr 1; 43(4):1921-5. PMID: 6831427
15. Sobko T, Reinders CI, Jansson E, Norin E, Midtvedt T, Lundberg JM. Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite. Nitric Oxide. 2005 Dec; 13(4):272-8. PMID: 16183308
16. Sobko T, Huang L, Midtvedt T, Norin E, Gustafsson LE, Norman M, et al. Generation of NO by probiotic bacteria in the gastrointestinal tract. Free Radical Biology and Medicine. 2006 Sep; 41(6):985-91. PMID: 16934682
17. Sparacino-Watkins C, Stolz JF, Basu P. Nitrate and periplasmic nitrate reductases. Chem Soc Rev. The Royal Society of Chemistry; 2013; 43(2):676-706.
18. Simon J. Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev. 2002 Aug; 26(3):285-309. PMID: 12165429
19. Espey MG. Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota. Free Radical Biology and Medicine. Elsevier; 2013 Feb 1; 55(C):130-40.
20. Marteyn B, Scorza FB, Sansonetti PJ, Tang C. Breathing life into pathogens: the influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract. Cellular Microbiology. Blackwell Publishing Ltd; 2010 Dec 19; 13(2):171-6. doi: 10.1111/j.1462-5822.2010.01549.x PMID: 21166974
21. He G, Shankar RA, Chzhan M, Samouilov A, Kuppusamy P, Zweier JL. Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. PNAS. 1999 Apr 13; 96(8):4586-91. PMID: 10200306
22. MacArthur PH, Shiva S, Gladwin MT. Measurement of circulating nitrite and S-nitrosothiols by reductive chemiluminescence. J Chromatogr B Analyt Technol Biomed Life Sci. 2007 May 15; 851(1-2):93-105. PMID: 17400039
23. Tiso M, Tejero J, Kenney CT, Frizzell S, Gladwin MT. Nitrite reductase activity of nonsymbiotic hemoglobins from Arabidopsis thaliana. Biochemistry. 2012 Jul 3; 51(26):5285-92. PMID: 22620259
24. Jones SA, Chowdhury FZ, Fabich AJ, Anderson A, Schreiner DM, House AL, et al. Respiration of Escherichia coli in the mouse intestine. Infection and Immunity. 2007 Oct 1; 75(10):4891-9. PMID: 17698572
25. Jia W, Cole J. Nitrate and nitrite transport in Escherichia coli. Biochem Soc Trans. 2005 Feb; 33(Pt 1):159-61.
26. Wolf G, Arendt EK, Pfähler U, Hammes WP. Heme-dependent and heme-independent nitrite reduction by lactic acid bacteria results in different N-containing products. Int J Food Microbiol. 1990 May; 10(3-4):323-9. PMID: 2397162
27. Brooijmans RJW, de Vos WM, Hugenholtz J. Lactobacillus plantarum WCFS1 electron transport chains. Applied and Environmental Microbiology. American Society for Microbiology; 2009 Jun; 75 (11):3580-5. doi: 10.1128/AEM.00147-09 PMID: 19346351
28. Bueno E, Mesa S, Bedmar EJ, Richardson DJ, Delgado MJ. Bacterial Adaptation of Respiration from Oxic to Microoxic and Anoxic Conditions: Redox Control. Antioxidants & Redox Signaling. 2012 Apr 15; 16(8):819-52.
29. Stewart V. Regulation of nitrate and nitrite reductase synthesis in enterobacteria. Antonie Van Leeuwenhoek. 1994; 66(1-3):37-45. PMID: 7747936
30. Ji XB, Hollocher TC. Reduction of nitrite to nitric oxide by enteric bacteria. Biochem Biophys Res Commun. 1988 Nov 30; 157(1):106-8. PMID: 3058123
31. Ji XB, Hollocher TC. Nitrate Reductase of Escherichia-Coli as a No-Producing Nitrite Reductase. Biochemical Archives. 1989 Feb; 5(1):61-6.
32. Xu J, Verstraete W. Evaluation of nitric oxide production by lactobacilli. Appl Microbiol Biotechnol. Springer-Verlag; 2001 Aug 1; 56(3-4):504-7.
33. Corker H, Poole RK. Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp. Journal of Biological Chemistry. American Society for Biochemistry and Molecular Biology; 2003 Aug 22; 278(34):31584-92. PMID: 12783887
34. Vermeiren J, Van de Wiele T, Verstraete W, Boeckx P, Boon N. Nitric oxide production by the human intestinal microbiota by dissimilatory nitrate reduction to ammonium. Journal of Biomedicine and Biotechnology. Hindawi Publishing Corporation; 2009; 2009(4):284718-10. doi: 10.1155/2009/284718 PMID: 19888436
35. Sears CL. A dynamic partnership: Celebrating our gut flora. Anaerobe. 2005 Oct; 11(5):247-51. PMID: 16701579
36. O'Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006 Jul; 7(7):688-93. PMID: 16819463
37. Flint HJ, O'Toole PW, Walker AW. Special issue: The Human Intestinal Microbiota. Microbiology (Reading, Engl). 2010 Nov; 156(Pt 11):3203-4. doi: 10.1099/mic.0.045443-0 PMID: 21045216
38. Leser TD, Mølbak L. Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environmental Microbiology. Blackwell Publishing Ltd; 2009 Sep; 11 (9):2194-206. doi: 10.1111/j.1462-2920.2009.01941.x PMID: 19737302
39. Unden G, Bongaerts J. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta. 1997 Jul 4; 1320(3):217-34. PMID: 9230919
40. Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V, Keestra AM, et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science. American Association for the Advancement of Science; 2013 Feb 8; 339(6120):708-11. doi: 10.1126/science.1232467 PMID: 23393266
41. Siezen RJ, van Hylckama Vlieg JET. Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb Cell Fact. 2011 Aug 30; 10 Suppl 1(Suppl 1):S3. doi: 10.1186/1475-2859-10-S1-S3 PMID: 21995294
42. Jones JA, Ninnis JR, Hopper AO. Nitrite and Nitrate Concentrations and Metabolism in Breast Milk, Infant Formula, and Parenteral Nutrition. Journal of Parenteral . . .. 2013.
43. Gates AJ, Hughes RO, Sharp SR, Millington PD, Nilavongse A, Cole J, et al. Properties of the periplasmic nitrate reductases from Paracoccus pantotrophus and Escherichia coli after growth in tungsten-supplemented media. FEMS Microbiol Lett. 2003 Mar 28; 220(2):261-9. PMID: 12670690
44. Cole J. Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol Lett. 1996 Feb 1; 136(1):1-11. PMID: 8919448
45. Carlström M, Larsen FJ, Nyström T, Hezel M, Borniquel S, Weitzberg E, et al. Dietary inorganic nitrate reverses features of metabolic syndrome in endothelial nitric oxide synthase-deficient mice. Proc Natl Acad Sci USA. 2010 Oct 12; 107(41):17716-20. doi: 10.1073/pnas.1008872107 PMID: 20876122
46. Schreiber F, Stief P, Gieseke A, Heisterkamp IM, Verstraete W, de Beer D, et al. Denitrification in human dental plaque. BMC Biol. BioMed Central Ltd; 2010; 8(1):24.
47. Jones GA. Dissimilatory metabolism of nitrate by the rumen microbiota. Can J Microbiol. 1972; 18 (12):1783-7. PMID: 4675328
48. Sindelar JJ, Milkowski AL. Human safety controversies surrounding nitrate and nitrite in the diet. Nitric Oxide. 2012 May; 26(4):259-66. doi: 10.1016/j.niox.2012.03.011 PMID: 22487433
49. McKnight GM, Duncan CW, Leifert C, Golden MH. Dietary nitrate in man: friend or foe? British Journal of Nutrition. Cambridge University Press; 1999 May 1; 81(05):349-58.
50. Vince A, Dawson AM, Park N, O'Grady F. Ammonia production by intestinal bacteria. Gut. 1973 Mar; 14(3):171-7. PMID: 4573343
51. Cole J. Independent pathways for the anaerobic reduction of nitrite to ammonia by Escherichia coli. Biochem Soc Trans. 1982 Dec; 10(6):476-8. PMID: 6295832
52. Auron A, Brophy PD. Hyperammonemia in review: pathophysiology, diagnosis, and treatment. Pediatr Nephrol. Springer-Verlag; 2012 Feb 1; 27(2):207-22. doi: 10.1007/s00467-011-1838-5 PMID: 21431427
53. Hadjihambi A, Khetan V, Jalan R. Pharmacotherapy for hyperammonemia. Expert Opin Pharmacother. 2014 Aug; 15(12):1685-95. doi: 10.1517/14656566.2014.931372 PMID: 25032885
54. Kundra A, Jain A, Banga A, Bajaj G, Kar P. Evaluation of plasma ammonia levels in patients with acute liver failure and chronic liver disease and its correlation with the severity of hepatic encephalopathy and clinical features of raised intracranial tension. Clin Biochem. 2005 Aug; 38(8):696-9. PMID: 15963970
55. Strauss E, Gomes de Sá Ribeiro M de F. Bacterial infections associated with hepatic encephalopathy: prevalence and outcome. Ann Hepatol. 2003 Jan; 2(1):41-5. PMID: 15094705
56. Patil DH, Westaby D, Mahida YR, Palmer KR, Rees R. Comparative modes of action of lactitol and lactulose in the treatment of hepatic encephalopathy. Gut. 1987.
57. Vince A, Zeegen R, Drinkwater JE, O'Grady F, Dawson AM. The effect of lactulose on the faecal flora of patients with hepatic encephalopathy. J Med Microbiol. 1974 May; 7(2):163-8. PMID: 4600290