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Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions
Open accessAbstract
The biological nitrogen cycle involves step-wise reduction of nitrogen oxides to ammonium salts and oxidation of ammonia back to nitrites and nitrates by plants and bacteria. Neither process has been thought to have relevance to mammalian physiology; however in recent years the salivary bacterial reduction of nitrate to nitrite has been recognized as an important metabolic conversion in humans. Several enteric bacteria have also shown the ability of catalytic reduction of nitrate to ammonia via nitrite during dissimilatory respiration; however, the importance of this pathway in bacterial species colonizing the human intestine has been little studied. We measured nitrite, nitric oxide (NO) and ammonia formation in cultures of Escherichia coli, Lactobacillus and Bifidobacterium species grown at different sodium nitrate concentrations and oxygen levels. We found that the presence of 5 mM nitrate provided a growth benefit and induced both nitrite and ammonia generation in E.coli and L.plantarum bacteria grown at oxygen concentrations compatible with the content in the gastrointestinal tract. Nitrite and ammonia accumulated in the growth medium when at least 2.5 mM nitrate was present. Time-course curves suggest that nitrate is first converted to nitrite and subsequently to ammonia. Strains of L.rhamnosus, L.acidophilus and B.longum infantis grown with nitrate produced minor changes in nitrite or ammonia levels in the cultures. However, when supplied with exogenous nitrite, NO gas was readily produced independently of added nitrate. Bacterial production of lactic acid causes medium acidification that in turn generates NO by non-enzymatic nitrite reduction. In contrast, nitrite was converted to NO by E.coli cultures even at neutral pH. We suggest that the bacterial nitrate reduction to ammonia, as well as the related NO formation in the gut, could be an important aspect of the overall mammalian nitrate/nitrite/NO metabolism and is yet another way in which the microbiome links diet and health.
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TL;DR
In vitro cultures of common gut bacteria show that nitrate can be reduced first to nitrite and then to ammonia under oxygen and nitrate conditions relevant to the gastrointestinal tract. E. coli and L. plantarum were the main nitrate reducers, while lactic acid bacteria also generated NO from nitrite largely through acid-driven non-enzymatic reduction.
Key findings
- E. coli and L. plantarum grown with 5 mM nitrate at low oxygen showed a growth benefit and produced nitrite and ammonia; nitrite and ammonia accumulated when nitrate was at least 2.5 mM, reaching about 260 μM NO2− and 180 μM NH4+ in E. coli media at 5–20 mM nitrate.
- Time-course experiments at 2% O2 with 5 mM nitrate suggested nitrate is first converted to nitrite and subsequently to ammonia; nitrite peaked at 30–36 h at about 0.4 mM for E. coli and 0.1 mM for L. plantarum.
- L. rhamnosus, L. acidophilus and B. longum infantis showed minor changes in nitrite or ammonia with nitrate, but all LAB cultures produced NO from exogenous nitrite; LAB lactic acid acidified the medium and drove non-enzymatic nitrite reduction to NO, whereas E. coli converted nitrite to NO even at neutral pH.
- E. coli NO production from nitrite was low at 2% O2 (<40 ppb/109 CFU) and much larger after anaerobic growth, roughly correlating with increasing nitrate; arginine and L-NAME did not change NO production, arguing against bacterial NOS activity.
Methods
- In vitro cultures of E. coli (MG1655 in Results; Table 1 lists MG1566), L. acidophilus ATCC 4356, L. plantarum ATCC BAA-793 (WCFS1), L. rhamnosus ATCC 7469, and B. longum infantis ATCC 15697 were grown at 37°C in modified LMRS broth without ammonium citrate, with controlled O2 levels from 0% to 21% and nitrate from 0 to 20 mM; LAB were supplemented with heme and vitamin K2.
- Nitrite was measured by acidic tri-iodide-based gas-phase chemiluminescence, ammonia by colorimetric kits, NO gas by ozone-based chemiluminescence, and lactic acid enzymatically.
- Experiments were performed in triplicate, values reported as mean ± SD, nitrite and ammonia normalized to OD600 after 24 h growth, and one-way ANOVA used where applicable.
Limitations
- The paper states that the importance of this pathway in vivo demands further studies, that how much ammonia comes from nitrate-nitrite reduction versus deamination or urease activity requires detailed animal and/or human metabolic studies, and that the biological significance of dietary nitrate conversion in the intestinal lumen remains to be established.
- The paper notes that very little information exists on in vivo O2 concentrations in intestinal fluids, so the oxygen conditions used are approximations of gastrointestinal levels.
- Evident from the text: findings are from in vitro single-strain cultures, not complex gut communities or host tissue; ammonia measurements in cell pellets had large errors and possible ammonia evaporation, leading the authors to measure nitrate metabolites mainly in cell-free supernatant.
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In the paper
“We found that the presence of 5 mM nitrate provided a growth benefit and induced both nitrite and ammonia generation in E.coli and L.plantarum bacteria grown at oxygen concentrations compatible with the content in the gastrointestinal tract.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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In the paper
“In contrast, nitrite was converted to NO by E.coli cultures even at neutral pH.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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In the paper
“Nitrate concentrations equal to or above 2.5 mM had a significant effect on nitrite and ammonia production only in the L.plantarum cultures.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
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In the paper
“However, when supplied with exogenous nitrite, NO gas was readily produced independently of added nitrate.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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In the paper
“We found that the presence of 5 mM nitrate provided a growth benefit and induced both nitrite and ammonia generation in E.coli and L.plantarum bacteria grown at oxygen concentrations compatible with the content in the gastrointestinal tract.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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In the paper
“The presence of 5 mM nitrate provided a clear growth benefit to E.coli cultures maintained at 2% O2 or in anaerobic conditions (red lines with open symbols) and partially restored the growth to levels found in the aerobic conditions.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Effect of nitrate and oxygen on the growth patterns of E.coli in LMRS
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In the paper
“Nitrite and ammonia concentrations remained steady when nitrate concentrations were lower or equal to 1.0 mM.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Effect of oxygen on E.coli production of nitrite and ammonia from nitrate
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In the paper
“Strains of L.rhamnosus, L.acidophilus and B.longum infantis grown with nitrate produced minor changes in nitrite or ammonia levels in the cultures.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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In the paper
“Lysis by brief sonication in fresh media of the LAB cells to extract the cytosolic enzymes did not restored the generation of NO after injection of nitrite.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“1) E.coli, a facultative anaerobe, convert nitrate to nitrite and subsequently to ammonia which progressively accumulates in culture media”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion
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- It may state two separate claims as one. 32
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In the paper
“However when the O2 tension was 4% or lower nitrite and ammonia were both generated and excreted in the media and reached the highest concentrations in cultures grown under anaerobic conditions.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
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“Under 2% O2 small amounts of NO (< 40 ppb/109 CFU) were detected almost independently from the concentration of nitrate supplied.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“We found that nitrite concentrations begun to increase within 3 to 6 hours after nitrate addition and accumulated steadily to reach a maximum in 30–36 h at about 0.4 mM for E.coli and 0.1 mM for L.plantarum (Fig. 3A).”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Time-course of concurrent nitrite and ammonia formation
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“Similarly the ammonia concentrations plotted in Fig. 3B show well the almost linear and continuous increase measured between 9 and 30 h in both species but with different rates.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Time-course of concurrent nitrite and ammonia formation
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In the paper
“A smaller, but still considerable, effect on nitrite generation was observed in L.rhamnosus and L.acidophilus cultures and no significant changes were measured in B.longum infantis.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
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- Rests on an assumption: The O2 level of 2% used in some experiments is similar to the partial pressure found on the luminal surface of the intestinal mucosa.
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In the paper
“Inversely, much larger quantities were measured in analogous experiments after anaerobic growth and the response roughly correlated with the increasing nitrate concentrations.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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“Of particular note, nitrite concentration in L.plantarum increased until around 30 h and afterwards begun to decrease while ammonia kept increasing further.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Time-course of concurrent nitrite and ammonia formation
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“LAB cultures are well known to produce substantial acidification of the media due to the fermentation of glucose primarily to lactic acid and we confirmed its formation in large amounts (mM) by direct detection.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“The initial pH (6.5) decreased variably to values between 3.9 and 5.0 depending on the LAB species and the difference was the least for L. plantarum.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“However, when nitrate reached 2.5 mM both metabolites accumulated in the media and their concentrations were greatly increased and reached a maximum in the range 5–20 mM nitrate (to around 260 μM for NO2 − and 180 μM for NH4 +).”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Effect of oxygen on E.coli production of nitrite and ammonia from nitrate
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“This procedure resulted in the almost complete halt of NO generation in all LAB (solid bars in Fig. 4B) but only partially in E.coli cultures.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“Of note, cultures of B. longum infantis did not grow at, or above, 6% O2 and showed negligible content of nitrite and low ammonia independent of the oxygen level.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
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In the paper
“All the cultures produced a considerable but variable amount of NO after 100 μM nitrite injection, while the same addition to fresh LMRS, with or without nitrate, had no effect (bars with oblique lines).”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“LAB cultures that grew at O2 levels equivalent or greater than 6% showed no significant changes in nitrite or ammonia.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
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In the paper
“Replacing the growth media with fresh LMRS (pH = 6.5) almost completely blocked the LAB cultures ability to convert nitrite to NO but not in E.coli.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion > Physiological significance of NO formation by bacterial nitrate reduction
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In the paper
“This NO generation, however is greatly reduced at 2% oxygen and become nitrate independent.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion > Physiological significance of NO formation by bacterial nitrate reduction
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In the paper
“Our results also excluded the presence of active NOS enzymes in E.coli and L.plantarum”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion > Nitrogen oxides reduction pathways in the human gut
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In the paper
“Alongside with transport E.coli expresses two nitrite reductase enzymes (Nrf and Nir) that detoxify NO2 - by rapidly converting it to ammonia through a six-electron reduction [18].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Effect of oxygen on E.coli production of nitrite and ammonia from nitrate
What the sources say
- Not checked yetcites [18] J Simon, 2002, Enzymology and bioenergetics of respiratory nitrite ammonification, FEMS Microbiol Rev source
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In the paper
“a concentration compatible with levels found in the upper intestinal tract of healthy volunteers and with values measured in the mouse intestinal mucus [24].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Effect of nitrate and oxygen on the growth patterns of E.coli in LMRS
What the sources say
- Not checked yetcites [24] SA Jones, 2007, Respiration of Escherichia coli in the mouse intestine, Infection and Immunity source
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None of the sources cited for this claim have been checked yet.
In the paper
“The E.coli genome encodes at least three distinct nitrate reductase enzymes [4] that are known to be expressed during anaerobic respiration [17].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Effect of oxygen on E.coli production of nitrite and ammonia from nitrate
What the sources say
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We suggest that the bacterial nitrate reduction to ammonia, as well as the related NO formation in the gut, could be an important aspect of the overall mammalian nitrate/nitrite/NO metabolism and is yet another way in which the microbiome links diet and health.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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- Rests on an assumption: Ammonia generated by gut microbiota from nitrate would likely be carried to the liver via the portal vein and enter the urea cycle to be converted into urea and amino acids.
In the paper
“However, over the past 30 years it has been shown that many Lactobacilli species can incorporate heme from the environment and utilize menaquinones, also known as vitamins K, to eventually perform respiration [26].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
What the sources say
- Not checked yetcites [26] G Wolf, 1990, Heme-dependent and heme-independent nitrite reduction by lactic acid bacteria results in different N-containing products, Int J Food Microbiol source
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Bacterial production of lactic acid causes medium acidification that in turn generates NO by non-enzymatic nitrite reduction.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Abstract
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“These results indicate that at least 2 processes producing NO are present in E.coli: one predominates at 2% O2 tension and the other in anaerobic atmosphere.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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In the paper
“Brooijmans et al. [27] have also recently reported that exogenous addition of menaquinone 4 (vitamin K2) along with heme stimulate nitrate reduction in L.plantarum.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > Nitrate reduction by lactic acid bacteria cultures
What the sources say
- Not checked yetcites Brooijmans et al. [27] RJW Brooijmans, 2009, Lactobacillus plantarum WCFS1 electron transport chains, Applied and Environmental Microbiology source
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Many enteric bacteria are also capable of catalytic reduction of nitrate to N2 gas (denitrification) under anaerobic conditions, or to ammonia via two-steps dissimilatory or assimilatory pathways [17,18].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Introduction
What the sources say
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In the paper
“However, several following studies on bacterial NO formation have proposed different mechanisms independent of respiratory denitrification such as arginine dependent bacterial NOS enzymatic activity, DNRA and non-enzymatic processes [15,32–34].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
What the sources say
- Not checked yetcites [15] T Sobko, 2005, Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite, Nitric Oxide source
- Not checked yetcites [32] J Xu, 2001, Evaluation of nitric oxide production by lactobacilli, Appl Microbiol Biotechnol source
- Not checked yetcites [33] H Corker, 2003, Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp, Journal of Biological Chemistry source
- Not checked yetcites [34] J Vermeiren, 2009, Nitric oxide production by the human intestinal microbiota by dissimilatory nitrate reduction to ammonium, Journal of Biomedicine and Biotechnology
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“In 1988, Ji and Hollocher first observed the generation of NO from nitrite by E.coli in anaerobic conditions [30] and later concluded that nitrite-dependent NO production was due to the activity of the respiratory membrane-associated nitrate reductase enzymes [31].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
What the sources say
- Not checked yetcites [30] XB Ji, 1988, Reduction of nitrite to nitric oxide by enteric bacteria, Biochem Biophys Res Commun source
- Not checked yetcites [31] XB Ji, 1989, Nitrate Reductase of Escherichia-Coli as a No-Producing Nitrite Reductase, Biochemical Archives
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We concluded that LAB production of lactic acid causes sufficient medium acidification to induce the chemical nitrite conversion to NO”
- Also stated in: § Discussion · plain
“4) All LAB cultures examined generate large amounts of lactic acid causing sufficient acidification of culture media to drive nitrite disproportionation to NO.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
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- Also stated in: § Discussion · plain
None of the sources cited for this claim have been checked yet.
In the paper
“Recent and past data have demonstrated that nitrate-rich diets increase plasma and tissue levels of nitrite [9,10], but this cannot be accounted solely by nitrate reduction from oral bacteria and other mechanisms have been implicated and are under investigation [11].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Introduction
What the sources say
- Not checked yetcites [9] M Govoni, 2008, The increase in plasma nitrite after a dietary nitrate load is markedly attenuated by an antibacterial mouthwash, Nitric Oxide source
- Not checked yetcites [10] NJH Raat, 2009, Dietary nitrate and nitrite modulate blood and organ nitrite and the cellular ischemic stress response, Free Radical Biology and Medicine source
- Not checked yetcites [11] E Weitzberg, 2013, Novel aspects of dietary nitrate and human health, Annu Rev Nutr source
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“instead this process in E.coli is enzymatic and occurs around pH 6.5.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Results > NO production by bacterial cell suspensions
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“More recently, the normal bacterial flora has been shown to generate NO and gut luminal NO levels have been measured in vivo in rats [15,16].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Introduction
What the sources say
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“In healthy individuals dietary nitrate is usually well absorbed in the upper intestinal tract, however a considerable fraction of the daily nitrate intake (about 1/3) was found to reach the lower intestine while only 1% of it is recovered in the feces [12].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Introduction
What the sources say
- Not checked yetcites [12] B Bartholomew, 1984, The pharmacology of dietary nitrate and the origin of urinary nitrate, Food Chem Toxicol source
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Respiratory denitrification can also generate small but relevant amounts of NO as an intermediate product and has been implicated in the bacterial NO production in the gut [32,33].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion > Nitrogen oxides reduction pathways in the human gut
What the sources say
- Not checked yetcites [32] J Xu, 2001, Evaluation of nitric oxide production by lactobacilli, Appl Microbiol Biotechnol source
- Not checked yetcites [33] H Corker, 2003, Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp, Journal of Biological Chemistry source
Strength:plain· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
In the paper
“Sobko et al. [15] showed that in contrast to conventional rats, NO levels in the intestine of germ-free rats are extremely low and when inoculated with normal bacteria flora the observed NO production increased 10 fold.”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion > Physiological significance of NO formation by bacterial nitrate reduction
What the sources say
- Not checked yetcites [15] T Sobko, 2005, Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite, Nitric Oxide source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“it is well known that E.coli K12 strains express three molybdenum-containing nitrate reductases [17]”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion
What the sources say
- Not checked yetcites [17] C Sparacino-Watkins, 2013, Nitrate and periplasmic nitrate reductases, Chem Soc Rev source
Strength:boosted· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Cole and colleagues reported that the major product of nitrite reduction in E.coli is ammonia with about only 1% being reduced to NO at neutral pH [51].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion > Physiological implications of bacterial ammonia formation for health
What the sources say
- Not checked yetcites [51] J Cole, 1982, Independent pathways for the anaerobic reduction of nitrite to ammonia by Escherichia coli, Biochem Soc Trans source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“unique to this species, genes that encode a putative nitrate-reductase system (narGHJI) were recently identified in the L. plantarum WCFS1 genome, which suggests that it is capable of using nitrate as an electron acceptor [27].”
§ Nitrate Reduction to Nitrite, Nitric Oxide and Ammonia by Gut Bacteria under Physiological Conditions > Discussion
What the sources say
- Not checked yetcites [27] RJW Brooijmans, 2009, Lactobacillus plantarum WCFS1 electron transport chains, Applied and Environmental Microbiology source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
The paper relies on this without support.
The O2 level of 2% used in some experiments is similar to the partial pressure found on the luminal surface of the intestinal mucosa.
“with the O2 level fixed at 2%, a partial pressure similar to the one found on the luminal surface of the intestinal mucosa”
The paper relies on this without support.
Ammonia generated by gut microbiota from nitrate would likely be carried to the liver via the portal vein and enter the urea cycle to be converted into urea and amino acids.
“The ammonia thus generated would likely be carried to the liver via the portal vein, where it can enter the urea cycle and be converted into urea and amino acids.”
The paper relies on this without support.
The in vitro conditions used are compatible with nitrate-rich diets and oxygen levels found on the mucosal surfaces of the GI tract.
“using in vitro conditions compatible with nitrate-rich diets and oxygen levels found on the mucosal surfaces of the GI tract”
The paper relies on this without support.
The intestinal pH ranges between 5.7 and 7.5.
“Measurements of the intestine pH ranges between 5.7 and 7.5”
The paper relies on this without support.
Approximately 60% of an ingested nitrate dose in humans is not accounted for in excreted nitrogen-containing compounds.
“the biological fate of exogenous nitrate could not be accounted for in the excreted nitrogen-containing compounds which amount to approximately 60% of an ingested nitrate dose in humans”
The paper relies on this without support.
The bacterial species and strains studied in vitro are representative of those performing nitrate reduction in the human gut.
“selected common bacterial species colonizing the human intestine”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Nitrite can exert pH-dependent antimicrobial effects[204,232,233] via formation of reactive secondary nitrogen oxides that can disrupt aerobic respiration[234], inhibit bacterial acid production, and disrupt biofilm formation[235–237].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“In a recent set of experiments using gut facultative anaerobes, Escherichia coli and several Lactobacillus sp., there was an increase in the expression of nitrate reductase enzymes, an increase in nitrite formation, and a clear growth benefit in the setting of adequate nitrate as oxygen concentration decreases below 4% [233].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“Second, diffusion of oxygen from the enteral vasculature through the submucosal tissue and into the intestinal lumen creates an incredibly steep oxygen gradient, ranging from 80–100mmHg (~10–13%) in the submucosa and base of the villi, down to only 8–10mmHg (~1–2%) in the overlying mucus layer and an essentially anaerobic luminal center (Figure 4)[233,267].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“the majority of nitrate and nitrite are absorbed in the proximal small intestine[233,270].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“it is unlikely they significantly contribute to the enterosalivary circulation given that the majority of nitrate and nitrite are absorbed in the proximal small intestine[233,270].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“Yet, despite these localized, periodontal effects on microbial populations, high salivary nitrite concentrations may also exert antimicrobial effects elsewhere in the oral cavity and gut, possibly disrupting community composition or function of biologically beneficial populations of nitrate-reducing bacteria[204,232–237].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“Elevated rates of generation of these oxidative inflammatory mediators can have direct effects on enterocytes and mucosal integrity, impair NO-dependent vascular function, reduce nitrate and nitrite absorption, and exert selective pressure on bacteria by augmenting innate anti-bacterial effects[204,233,321–324].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“Many bacteria are capable of reducing nitrate to nitrite to NO via the denitrification pathway.”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“commensal gut bacteria are able to directly produce NO and also modify NO production, potentially influencing regional blood flow, mucosal integrity, microbial diversity, and effective nitrate and nitrite uptake.”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“both Lactobacilli and Bifidobacteria have been shown to generate NO from nitrite in culture”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
In the citing paper
“while Lactobacilli, Escherichia coli and Salmonella typhimurium all increase cecal NO production when supplied with nitrate[217,233,271,278].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [233]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
E. coli strain identifier differs between Table 1 and the results
MinorTable 1 identifies the E. coli strain used in the study as MG1566, whereas the results identify the strain in the growth experiments as MG1655. The text does not establish whether these are different strains or a mislabeled strain.
“| Escherichia coli | MG1566 | 7.6 | ND c |”
“We first compared E.coli MG1655 strain growth patterns”
Citations
Cites
The gut flora as a forgotten organ
O'Hara, A. M., & Shanahan, F. (2006) · The EMBO Reports · doi:10.1038/sj.embor.7400731 · Cited by 2,791
The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics
Lundberg, J. O., Weitzberg, E., & Gladwin, M. T. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2466 · Cited by 2,739 · cited 1×
“Nitrate (NO3 ) and nitrite (NO2 ) anions have long been identified as stable products of NO oxidation, but in recent years the nitrate— nitrite—nitric oxide reductive pathway has emerged as an alternative route to the classical enzymatic NO formation by oxidation of L-arginine with molecular oxygen [2,3].”
BackgroundNitric oxide : biology and pathobiology
Ignarro, L. J. (2000) · Cited by 1,306
Host-Derived Nitrate Boosts Growth of E. coli in the Inflamed Gut
Winter, S. E., Winter, M. G., Xavier, M. N., Thiennimitr, P., Poon, V., Keestra, A. M., Laughlin, R. C., Gomez, G., Wu, J., Lawhon, S. D., et al. (2013) · Science · doi:10.1126/science.1232467 · Cited by 1,019
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Nitrate, bacteria and human health
Lundberg, J. O., Weitzberg, E., Cole, J. A., & Benjamin, N. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro929 · Cited by 739
Govoni, M., Jansson, E. Å., Weitzberg, E., & Lundberg, J. O. (2008) · Nitric Oxide · doi:10.1016/j.niox.2008.08.003 · Cited by 602
Nitrate Synthesis in the Germfree and Conventional Rat
Green, L. C., Tannenbaum, S. R., & Goldman, P. (1981) · Science · doi:10.1126/science.6451927 · Cited by 559
Nitrite as Regulator of Hypoxic Signaling in Mammalian Physiology
van Faassen, E. E., Bahrami, S., Feelisch, M., Hogg, N., Kelm, M., Kim‐Shapiro, D. B., Kozlov, A. V., Li, H., Lundberg, J. O., Mason, R., et al. (2009) · Medicinal Research Reviews · doi:10.1002/med.20151 · Cited by 435
Nitrate and periplasmic nitrate reductases
Sparacino-Watkins, C., Stolz, J. F., & Basu, P. (2014) · Chem. Soc. Rev. · doi:10.1039/c3cs60249d · Cited by 426 · cited 3×
“Many enteric bacteria are also capable of catalytic reduction of nitrate to N2 gas (denitrification) under anaerobic conditions, or to ammonia via two-steps dissimilatory or assimilatory pathways [17,18].”
Background
Flagged first, then by citations
Research works printed but not linked: 1
- XB Ji, 1989, Nitrate Reductase of Escherichia-Coli as a No-Producing Nitrite Reductase, Biochemical Archives, 5, 61
Cited by
Sorted by citations
Items 301–310 of 310
Keenan, S. W., Emmons, A. L., & DeBruyn, J. M. (2024) · Figshare · doi:10.6084/m9.figshare.26616526
Tian, X., Liu, Y., Tian, Y., Shao, L., Ma, Y., & Wang, W. (2025) · Journal of Food Science · doi:10.1111/1750-3841.70710
Xu, S., Raza, D., & Musarrat, M. (2026) · Food Chemistry Advances · doi:10.1016/j.focha.2026.101238
Kinstler, S. R., Lee, M. D., Wong, E. A., Cline, J. L., & Maurer, J. J. (2025) · Avian Diseases · doi:10.1637/aviandiseases-d-25-00080
Nitrate sustains oral microbiome function and gastric NO synthesis during antiseptic use
Paiva, B., Murta, B., Gonçalves, J., Bento, D., Lourenço, C. F., Laranjinha, J. A. N., Ledo, A., & Rocha, B. S. (2026) · Redox Experimental Medicine · doi:10.1530/rem-26-0007
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The oral cavity as a bioreactor in halitosis
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Metadata
- Authors
- Tiso, M., & Schechter, A. N.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Schechter, Alan N.
- ORCID
- Schechter, Alan N.
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-03-24
- Volume
- 10
- Issue
- 3
- Pages
- e0119712
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4372352
- OpenAlex
- W2016792399
- Semantic Scholar
- 85a9ecdb44af363910ac2a1b792ff39fd2cee804
- Cited by
- 311
- References
- 55
- Citations by year
- 2026: 8 · 2025: 30 · 2024: 41 · 2023: 39 · 2022: 27 · 2021: 32 · 2020: 43 · 2019: 22 · 2018: 32 · 2017: 21 · 2016: 11 · 2015: 4
- FWCI
- 9.85
- Type
- journal article
- Language
- en
- Update notices
- correction (2015-05-06)
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/publicdomain/zero/1.0/ (vor)
- Locations
- PLoS ONE (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- nitrate reduction, nitrite, nitric oxide, ammonia synthesis, gut microbiota, Escherichia coli, Lactobacillus, Bifidobacterium, lactic acid
- MeSH terms
- Gastrointestinal Microbiome, Ammonia, Analysis of Variance, Bifidobacterium, Escherichia coli, Humans, Lactobacillus, Nitrates, Nitric Oxide, Nitrites, Oxygen, Lactic Acid, Nitrogen Cycle
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