Managing the rumen to limit the incidence and severity of nitrite poisoning in nitrate-supplemented ruminants
J. V. Nolan A B , I. R. Godwin A , V. de Raphélis-Soissan A and R. S. Hegarty AA School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
B Corresponding author. Email: jnolan@une.edu.au
Animal Production Science 56(8) 1317-1329 https://doi.org/10.1071/AN15324
Submitted: 24 June 2015 Accepted: 13 November 2015 Published: 27 May 2016
Abstract
Inclusion of nitrate (NO3−) in ruminant diets is a means of increasing non-protein nitrogen intake while at the same time reducing emissions of enteric methane (CH4) and, in Australia, gaining carbon credits. Rumen microorganisms contain intracellular enzymes that use hydrogen (H2) released during fermentation to reduce NO3− to nitrite (NO2−), and then reduce the resulting NO2− to ammonia or gaseous intermediates such as nitrous oxide (N2O) and nitric oxide (NO). This diversion of H2 reduces CH4 formation in the rumen. If NO2− accumulates in the rumen, it may inhibit growth of methanogens and other microorganisms and this may further reduce CH4 production, but also lower feed digestibility. If NO2− is absorbed and enters red blood cells, methaemoglobin is formed and this lowers the oxygen-carrying capacity of the blood. Nitric oxide produced from absorbed NO2− reduces blood pressure, which, together with the effects of methaemoglobin, can, at times, lead to extreme hypoxia and death. Nitric oxide, which can be formed in the gut as well as in tissues, has a variety of physiological effects, e.g. it reduces primary rumen contractions and slows passage of digesta, potentially limiting feed intake. It is important to find management strategies that minimise the accumulation of NO2−; these include slowing the rate of presentation of NO3– to rumen microbes or increasing the rate of removal of NO2−, or both. The rate of reduction of NO3− to NO2− depends on the level of NO3− in feed and its ingestion rate, which is related to the animal’s feeding behaviour. After NO3− is ingested, its peak concentration in the rumen depends on its rate of solubilisation. Once in solution, NO3− is imported by bacteria and protozoa and quickly reduced to NO2−. One management option is to encapsulate the NO3− supplement to lower its solubility. Acclimating animals to NO3− is an established management strategy that appears to limit NO2− accumulation in the rumen by increasing microbial nitrite reductase activity more than nitrate reductase activity; however, it does not guarantee complete protection from NO2− poisoning. Adding concentrates into nitrate-containing diets also helps reduce the risk of poisoning and inclusion of microbial cultures with enhanced NO2−-reducing properties is another potential management option. A further possibility is to inhibit NO2− absorption. Animals differ in their tolerance to NO3− supplementation, so there may be opportunities for breeding animals more tolerant of dietary NO3−. Our review aims to integrate current knowledge of microbial processes responsible for accumulation of NO2− in rumen fluid and to identify management options that could minimise the risks of NO2− poisoning while reducing methane emissions and maintaining or enhancing livestock production.
Additional keywords: behaviour, greenhouse gas, methane, microbial processes, supplementation.
References
Alaboudi AR, Jones GA (1985) Effect of acclimation to high nitrate intakes on some rumen fermentation parameters in sheep. Canadian Journal of Animal Science 65, 841–849.| Effect of acclimation to high nitrate intakes on some rumen fermentation parameters in sheep.Crossref | GoogleScholarGoogle Scholar |
Allison MJ, Reddy CA (1984) Adaptations of gastrointestinal bacteria in response to changes in dietary oxalate and nitrate. In ‘Proceedings of the third international symposium on microbial ecology’. (Eds MJ Klug, CA Reddy) pp. 248–256. (American Society for Microbiology: Washington, DC)
Andrade SL, Einsle O (2013) The tricky task of nitrate/nitrite antiport. Angewandte Chemie International Edition 52, 10422–10424.
| The tricky task of nitrate/nitrite antiport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Cku73M&md5=9ec6ac625c3d80d6b07aaf5306b083aaCAS |
Andrew PJ, Mayer B (1999) Enzymatic function of nitric oxide synthases. Cardiovascular Research 43, 521–531.
| Enzymatic function of nitric oxide synthases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlslCksrc%3D&md5=76ad554cfdfa3a303d31acc681dafcb9CAS | 10690324PubMed |
Aschenbach JR, Bilk S, Tadesse G, Stumpff F, Gäbel G (2009) Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondiffusive uptake of acetate in the ruminal epithelium of sheep. American Journal of Physiology. Gastrointestinal and Liver Physiology 296, G1098–G1107.
| Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondiffusive uptake of acetate in the ruminal epithelium of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFagtrY%3D&md5=9663873647d9cf5d7055537134e8335dCAS | 19264953PubMed |
Ashbury AC, Rohde EA (1964) Nitrate intoxication in cattle: the effects of lethal doses of nitrite on blood pressure. American Journal of Veterinary Research 25, 1010–1013.
Barnett JA, Bowman IBR (1957) In vitro studies on the reduction of nitrate by rumen liquor. Journal of the Science of Food and Agriculture 8, 243–248.
| In vitro studies on the reduction of nitrate by rumen liquor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2sXlslKhug%3D%3D&md5=0a16d65db52d3b951d677726c0446c98CAS |
BRENDA (2015) ‘The comprehensive enzyme information system.’ Available at http://www.brenda-enzymes.org/enzyme.php?ecno=1.7.1.1 [Verified 14 June 2015]
Brittain T, Blackmore R, Greenwood C, Thomson AJ (1992) Bacterial nitrite-reducing enzymes. European Journal of Biochemistry 209, 793–802.
| Bacterial nitrite-reducing enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtVOmtrc%3D&md5=5cb01f3e6baaed8f2b689d9c2ea0341cCAS | 1425687PubMed |
Bruning-Fann JS, Kaneene JB (1993) The effects of nitrate, nitrite, and N-nitroso compounds on animal health. Veterinary and Human Toxicology 35, 237–253.
Bryan NS (2006) Nitrite in nitric oxide biology: cause or consequence?: A systems-based review. Free Radical Biology & Medicine 41, 691–701.
| Nitrite in nitric oxide biology: cause or consequence?: A systems-based review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotVyqsb4%3D&md5=9c2950b040295ea12400fccff60e2ac3CAS |
Burrows GE, Horn GW, McNew RW, Croy LI, Keeton RD, Kyle J (1987) The prophylactic effect of corn supplementation on experimental nitrate intoxication in cattle. Journal of Animal Science 64, 1682–1689.
Cabello P, Roldan MD, Moreno-Vivian C (2004) Nitrate reduction and the nitrogen cycle in archaea. Microbiology 150, 3527–3546.
| Nitrate reduction and the nitrogen cycle in archaea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVejs7jI&md5=d0f462eae4e0adfb16a08c344240bd8eCAS | 15528644PubMed |
Callaghan MJ, Tomkins NW, Benu I, Parker AJ (2014) How feasible is it to replace urea with nitrates to mitigate greenhouse gas emissions from extensively managed beef cattle? Animal Production Science 54, 1300–1304.
| How feasible is it to replace urea with nitrates to mitigate greenhouse gas emissions from extensively managed beef cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaktLnO&md5=00c0333ff7442f04e50495a9007c335bCAS |
Castro M, Munoz JM, Arruebo MP, Murillo MD, Arnal C, Bonafonte JI, Plaza MA (2012) Involvement of neuronal nitric oxide synthase (nNOS) in the regulation of migrating motor complex (MMC) in sheep. Veterinary Journal (London, England) 192, 352–358.
| Involvement of neuronal nitric oxide synthase (nNOS) in the regulation of migrating motor complex (MMC) in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFCgt7k%3D&md5=cf07b772890026c6c6be15d34074b1dfCAS |
Chaucheyras-Durand F, Masseglia S, Fonty G, Forano E (2010) Influence of the composition of the cellulolytic flora on the development of hydrogenotrophic microorganisms, hydrogen utilization, and methane production in the rumens of gnotobiotically reared lambs. Applied and Environmental Microbiology 76, 7931–7937.
| Influence of the composition of the cellulolytic flora on the development of hydrogenotrophic microorganisms, hydrogen utilization, and methane production in the rumens of gnotobiotically reared lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGks74%3D&md5=92bb905e2e462256888ead8e92963bb8CAS | 20971877PubMed |
Chen J, Godwin IR (2013) The effects of nitric oxide synthetase stimulation and inhibition on rumen motility in sheep. Recent Advances in Animal Nutrition in Australia 19, 29–30.
Cockrum RR, Austin KJ, Ludden PA, Cammack KM (2010) Effect of subacute dietary nitrate on production traits and plasma analytes in Suffolk ewes. Animal 4, 702–708.
| Effect of subacute dietary nitrate on production traits and plasma analytes in Suffolk ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVehtbw%3D&md5=3679dc61d6b8c01832fffea6636dd66aCAS | 22444122PubMed |
Conrad R, Wetter B (1990) Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria. Archives of Microbiology 155, 94–98.
| Influence of temperature on energetics of hydrogen metabolism in homoacetogenic, methanogenic, and other anaerobic bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvVKktA%3D%3D&md5=272cb2b3c55d442b7996a5de15891e95CAS |
Davidson WB, Dougherty JL, Bolton JL (1941) Nitrate poisoning of livestock. Canadian Journal of Comparative Medicine V, 303–313.
Dawson KA, Allison MJ (1988) Digestive disorders and nutritional toxicity. In ‘The rumen microbial ecosystem.’ (Ed. PN Hobson) pp. 445–459. (Elsevier Applied Science: London)
de Raphélis-Soissan V, Li L, Godwin IR, Barnett MC, Perdok HB, Hegarty RS (2014) Use of nitrate and Propionibacterium acidipropionici to reduce methane emissions and increase wool growth of Merino sheep. Animal Production Science 54, 1860–1866.
| Use of nitrate and Propionibacterium acidipropionici to reduce methane emissions and increase wool growth of Merino sheep.Crossref | GoogleScholarGoogle Scholar |
de Raphélis-Soissan V, Nolan JV, Newbold JR, Godwin IR, Hegarty RS (2016a) Animal production in Australia. Proceedings of the 31st biennial conference of the Australian Society of Animal Production 31, in press.
de Raphélis-Soissan V, Nolan JV, Newbold JR, Godwin IR, Hegarty RS (2016b) Can adaptation to nitrate supplementation and provision of fermentable energy reduce nitrite accumulation in rumen contents in vitro? Animal Production Science 56, 605–612.
| Can adaptation to nitrate supplementation and provision of fermentable energy reduce nitrite accumulation in rumen contents in vitro?Crossref | GoogleScholarGoogle Scholar |
DoE (2015) ‘Carbon farming initiative.’ (Department of the Environment, Australian Government) Available at http://www.environment.gov.au/climate-change/emissions-reduction-fund/carbon-farming-in [Verified 16 March 2016]
Duncan C, Dougall H, Johnston P, Green S, Brogan R, Leifert C, Smith L, Golden M, Benjamin N (1995) Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nature Medicine 1, 546–551.
| Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFegtb0%3D&md5=d1fa0faf99a372f83988555c9f5f8295CAS | 7585121PubMed |
Einsle O, Stach P, Messerschmidt A, Simon J, Kroger A, Huber R, Kroneck PM (2000) Cytochrome c nitrite reductase from Wolinella succinogenes. Structure at 1.6 A resolution, inhibitor binding, and heme-packing motifs. The Journal of Biological Chemistry 275, 39608–39616.
| Cytochrome c nitrite reductase from Wolinella succinogenes. Structure at 1.6 A resolution, inhibitor binding, and heme-packing motifs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptFSrtLw%3D&md5=b7ff02dac48d571d93e329ce6326cf42CAS | 10984487PubMed |
El-Zaiat HM, Araujo RC, Soltan YA, Morsy AS, Louvandini H, Pires AV, Patino HO, Correa PS, Abdalla AL (2014) Encapsulated nitrate and cashew nut shell liquid on blood and rumen constituents, methane emission, and growth performance of lambs. Journal of Animal Science 92, 2214–2224.
| Encapsulated nitrate and cashew nut shell liquid on blood and rumen constituents, methane emission, and growth performance of lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXot12itLk%3D&md5=d0cdb4e22cef200e439f5ab549372cb1CAS | 24663200PubMed |
Emerick RJ, Embry LB (1961) Effect of chlortetracycline on methemoglobinemia resulting from the ingestion of sodium bitrate by ruminants. Journal of Animal Science 20, 844–848.
Farra PA, Satter LD (1971) Manipulation of the ruminal fermentation. III. Effect of nitrate on ruminal volatile fatty acid production and milk composition. Journal of Dairy Science 54, 1018–1024.
| Manipulation of the ruminal fermentation. III. Effect of nitrate on ruminal volatile fatty acid production and milk composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXksVKgur4%3D&md5=f08c993c75e700bee1f7cc3da02d1176CAS |
Feelisch M, Fernandez BO, Bryan NS, Garcia-Saura MF, Bauer S, Whitlock DR, Ford PC, Janero DR, Rodriguez J, Ashrafian H (2008) Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and -scavenging systems. The Journal of Biological Chemistry 283, 33927–33934.
| Tissue processing of nitrite in hypoxia: an intricate interplay of nitric oxide-generating and -scavenging systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVelu7%2FO&md5=f04858b83d33521e8087514e808d4423CAS | 18835812PubMed |
Freer M, Dove H, Nolan JV (Eds) (2007) ‘Nutrient requirements of domesticated livestock.’ (CSIRO Publishing: Melbourne)
Friedman MA, Greene EJ, Epstein SS (1972) Rapid gastric absorption of sodium nitrite in mice. Journal of Pharmaceutical Sciences 61, 1492–1494.
| Rapid gastric absorption of sodium nitrite in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XlsF2qu7g%3D&md5=2290b1165e5836c8b0a3b845c16f738fCAS | 5068963PubMed |
Geurink JH, Malestein A, Kemp A, Klooster A (1979) Nitrate poisoning in cattle. 3. The relationship between nitrate intake with hay or fresh forage and the speed of intake on the formation of methaemoglobin. Netherlands Journal of Agricultural Science 27, 268–276.
Goddard AD, Moir JWB, Richardson DJ, Ferguson SJ (2008) Interdependence of two NarK domains in a fused nitrate/nitrite transporter. Molecular Microbiology 70, 667–681.
| Interdependence of two NarK domains in a fused nitrate/nitrite transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlChu73M&md5=1dbd5d372a6fffa2782811c1433117daCAS | 18823285PubMed |
Godwin IR, Li L, Luijben K, Oelbrandt N, Velazco J, Miller J, Hegarty RS (2015) The effects of chronic nitrate supplementation on erythrocytic methaemoglobin reduction in cattle. Animal Production Science 55, 611–616.
| The effects of chronic nitrate supplementation on erythrocytic methaemoglobin reduction in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsV2jtrw%3D&md5=26ad5fcfc659dece09f453a85802d0a7CAS |
Grudziński I (1991) Studies on the mechanism of the toxic action of sodium nitrite on intestinal absorption in rats. Archives of Environmental Contamination and Toxicology 21, 475–479.
| Studies on the mechanism of the toxic action of sodium nitrite on intestinal absorption in rats.Crossref | GoogleScholarGoogle Scholar | 1659336PubMed |
Guo WS, Schaefer DM, Guo XX, Ren LP, Meng QX (2009) Use of nitrate-nitrogen as a sole dietary nitrogen source to inhibit ruminal methanogenesis and to improve microbial nitrogen synthesis in vitro. Asian-Australasian Journal of Animal Sciences 22, 542–549.
| Use of nitrate-nitrogen as a sole dietary nitrogen source to inhibit ruminal methanogenesis and to improve microbial nitrogen synthesis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVeitLw%3D&md5=8149ab644f49c3bc7017be10322a9eb1CAS |
Harborne NR, Griffiths L, Busby SJ, Cole JA (1992) Transcriptional control, translation and function of the products of the five open reading frames of the Escherichia coli nir operon. Molecular Microbiology 6, 2805–2813.
| Transcriptional control, translation and function of the products of the five open reading frames of the Escherichia coli nir operon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xmt1OlurY%3D&md5=d13ca6b6e6ada01402b087043d400d67CAS | 1435259PubMed |
Holtenius P (1957) Nitrite poisoning in sheep, with special reference to the detoxification of nitrite in the rumen. Acta Agriculturae Scandinavica 7, 113–163.
| Nitrite poisoning in sheep, with special reference to the detoxification of nitrite in the rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2sXntlWluw%3D%3D&md5=be7ebd790cfd694915f6436baa511576CAS |
Hristov AN, Oh J, Lee C, Meinen R, Montes F, Ott T, Firkins J, Rotz A, Dell C, Adesogan A, Yang W, Tricarico J, Kebreab E, Waghorn G, Dijkstra J, Oosting S (2013) ‘Mitigation of greenhouse gas emissions in livestock production: a review of technical options for non-CO2 emissions.’ (Eds PJ Gerber, B Henderson, HPS Makkar) FAO Animal Production and Health Paper No. 177. (FAO: Rome)
Hristov AN, Oha J, Giallongo F, Frederick TW, Harper MT, Weeks HL, Branco AF, Moate PJ, Deighton MH, Richard S, Williams O, Kindermann M, Duval S (2015) An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production. Proceedings of the National Academy of Sciences 112, 10663–10668.
| An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1GrsL3P&md5=1c3d9175995aea8695a264f3f1772926CAS |
Hunault CC, van Velzen AG, Sips AJ, Schothorst RC, Meulenbelt J (2009) Bioavailability of sodium nitrite from an aqueous solution in healthy adults. Toxicology Letters 190, 48–53.
| Bioavailability of sodium nitrite from an aqueous solution in healthy adults.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSgtbnE&md5=f7bc56384571d43992cd67c217b22e1cCAS | 19576277PubMed |
Inderlied CB, Delwiche EA (1973) Nitrate reduction and the growth of Veillonella alcalescens. Journal of Bacteriology 114, 1206–1212.
Iwamoto M, Asanuma N, Hino T (2001) Effect of protozoa on nitrate and nitrite reduction in rumen microbiota. Kanto Journal of Animal Science 51, 9–15.
Iwamoto M, Asanuma N, Hino T (2002) Ability of Selenomonas ruminantium, Veillonella parvula, and Wolinella succinogenes to reduce nitrate and nitrite with special reference to the suppression of ruminal methanogenesis. Anaerobe 8, 209–215.
| Ability of Selenomonas ruminantium, Veillonella parvula, and Wolinella succinogenes to reduce nitrate and nitrite with special reference to the suppression of ruminal methanogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Chtrc%3D&md5=8fc2c7d82995f0ac7432d0da83074582CAS |
Jeyanathan J, Martin C, Morgavi DP (2014) The use of direct-fed microbials for mitigation of ruminant methane emissions: a review. Animal 8, 250–261.
| The use of direct-fed microbials for mitigation of ruminant methane emissions: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptlSisA%3D%3D&md5=08cfcf4da9fd55ccbd6fd5d974fdf5e5CAS | 24274095PubMed |
Jia W, Cole JA (2005) Nitrate and nitrite transport in Escherichia coli. Biochemical Society Transactions 33, 159–161.
| Nitrate and nitrite transport in Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovFyisA%3D%3D&md5=53c0860ab142e75147942b7b87ee854cCAS | 15667293PubMed |
Jones GA (1972) Dissimilatory metabolism of nitrate by the rumen microbiota. Canadian Journal of Microbiology 18, 1783–1787.
| Dissimilatory metabolism of nitrate by the rumen microbiota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXktVWqtw%3D%3D&md5=88f2dd2dd6aad158b73baef0a70d11bbCAS | 4675328PubMed |
Kern M, Simon J (2009) Periplasmic nitrate reduction in Wolinella succinogenes: cytoplasmic NapF facilitates NapA maturation and requires the menaquinol dehydrogenase NapH for membrane attachment. Microbiology 155, 2784–2794.
| Periplasmic nitrate reduction in Wolinella succinogenes: cytoplasmic NapF facilitates NapA maturation and requires the menaquinol dehydrogenase NapH for membrane attachment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGntrnM&md5=1023af77edeec0d6323e8ce1f0fcbd89CAS | 19477904PubMed |
Kern M, Volz J, Simon J (2011) The oxidative and nitrosative stress defence network of Wolinella succinogenes: cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide. Environmental Microbiology 13, 2478–2494.
| The oxidative and nitrosative stress defence network of Wolinella succinogenes: cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlans7zE&md5=15adcc65783d1e639b4a8aa0c6a9e232CAS | 21672122PubMed |
Kucera I (2005) Energy coupling to nitrate uptake into the denitrifying cells of Paracoccus denitrificans. Biochimica et Biophysica Acta 1709, 113–118.
| Energy coupling to nitrate uptake into the denitrifying cells of Paracoccus denitrificans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsVWhurs%3D&md5=c8e1fa23f7bf977353e5657fd06f1629CAS | 16112075PubMed |
Lee C, Beauchemin KA (2014) A review of feeding supplementary nitrate to ruminant animals: nitrate toxicity, methane emissions, and production performance. Canadian Journal of Animal Science 94, 557–570.
| A review of feeding supplementary nitrate to ruminant animals: nitrate toxicity, methane emissions, and production performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFejurzO&md5=3696d3a57a1a78e6d8eab852a50f808aCAS |
Lee C, Araujo RC, Koenig KM, Beauchemin KA (2015) Effects of encapsulated nitrate on enteric methane production and nitrogen and energy utilization in beef heifers. Journal of Animal Science 93, 2391–2404.
| Effects of encapsulated nitrate on enteric methane production and nitrogen and energy utilization in beef heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVCkt7fF&md5=2660976dc1cb9a62947f8f14b4ed9e3bCAS | 26020335PubMed |
Leng RA (2008) ‘The potential of feeding nitrate to reduce enteric methane production in ruminants.’ (Department of Climate Change: Canberra) Available at http://www.penambulbooks.com [Verified 16 March 2016]
Leng RA (2014) Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation. Animal Production Science 54, 519–543.
| Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXls1ehtrw%3D&md5=6de7aff9e7036dc759a4ca18856c995eCAS |
Lewicki J, Wiechetek M, Souffrant WB, Karlik W, Garwacki S (1998) The fate of nitrogen from 15N-labeled nitrate after a single intravenous administration of Na15NO3 in sheep. Canadian Journal of Physiology and Pharmacology 76, 850–857.
Lewis D (1951) The metabolism of nitrate and nitrite in the sheep. 1. The reduction of nitrate in the rumen of the sheep. The Biochemical Journal 48, 175–180.
| The metabolism of nitrate and nitrite in the sheep. 1. The reduction of nitrate in the rumen of the sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3MXjtVaktQ%3D%3D&md5=3108ac3858ba986f3eb2937596154305CAS | 14820824PubMed |
Lichtenwalner RE, Fontenot JP, Tucker RE (1973) Effect of source of supplemental nitrogen and level of nitrate on feedlot performance and vitamin A metabolism of fattening beef calves. Journal of Animal Science 37, 837–847.
| Effect of source of supplemental nitrogen and level of nitrate on feedlot performance and vitamin A metabolism of fattening beef calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXhtlyksw%3D%3D&md5=00cc05965a1322c011d2fe2d853c0c14CAS | 4795408PubMed |
Lin M, Schaefer DM, Guo WS, Ren LP, Meng QX (2011) Comparisons of in vitro nitrate reduction, methanogenesis, and fermentation acid profile among rumen bacterial, protozoal and fungal fractions. Asian-Australasian Journal of Animal Sciences 24, 471–478.
| Comparisons of in vitro nitrate reduction, methanogenesis, and fermentation acid profile among rumen bacterial, protozoal and fungal fractions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvFWlur4%3D&md5=ffdbc52a2940a5182207a22a4cc0fccfCAS |
Lin M, Guo W, Meng Q, Stevenson DM, Weimer PJ, Schaefer DM (2013) Changes in rumen bacterial community composition in steers in response to dietary nitrate. Applied Microbiology and Biotechnology 97, 8719–8727.
| Changes in rumen bacterial community composition in steers in response to dietary nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yltLjP&md5=21bc2ae9da356dc3800caef59ccf1bfbCAS | 23955503PubMed |
Lü W, Du J, Schwarzer NJ, Wacker T, Andrade SL, Einsle O (2013) The formate/nitrite transporter family of anion channels. Biological Chemistry 394, 715–727.
| The formate/nitrite transporter family of anion channels.Crossref | GoogleScholarGoogle Scholar | 23380538PubMed |
Luckmann M, Mania D, Kern M, Bakken LR, Frostegard A, Simon J (2014) Production and consumption of nitrous oxide in nitrate-ammonifying Wolinella succinogenes cells. Microbiology 160, 1749–1759.
| Production and consumption of nitrous oxide in nitrate-ammonifying Wolinella succinogenes cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVWlurjE&md5=9e70a78cb141a1e82822112214f091a1CAS | 24781903PubMed |
Lund P, Dahl R, Yang HJ, Hellwing ALF, Cao BB, Weisbjerg MR (2014) The acute effect of addition of nitrate on in vitro and in vivo methane emission in dairy cows. Animal Production Science 54, 1432–1435.
| The acute effect of addition of nitrate on in vitro and in vivo methane emission in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaktLvJ&md5=52fdc92b927383828abfa5248a3461d6CAS |
Lundberg JO (2008) Nitric oxide and the paranasal sinuses. Anatomical Record (Hoboken, N.J.) 291, 1479–1484.
| Nitric oxide and the paranasal sinuses.Crossref | GoogleScholarGoogle Scholar |
Lundberg JO, Weitzberg E, Gladwin MT (2008) The nitrate–nitrite–nitric oxide pathway in physiology and therapeutics. Nature Reviews. Drug Discovery 7, 156–167.
| The nitrate–nitrite–nitric oxide pathway in physiology and therapeutics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1Khsrw%3D&md5=654bf49a65046cb2e573a3b8e6ee9d1fCAS | 18167491PubMed |
Mamvura CI, Cho S, Mbiriri DT, Lee H, Choi H-J (2014) Effect of encapsulating nitrate in sesame gum on in vitro rumen fermentation parameters. Asian–Australasian Journal of Animal Sciences 27, 1577–1583.
| Effect of encapsulating nitrate in sesame gum on in vitro rumen fermentation parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVentrvI&md5=4e895f21b6e7a9df4fbeb5e335c903fbCAS | 25358317PubMed |
Marais JP, Therion JJ, Mackie RI, Kristner A, Dennison C (1988) Effect of nitrate and its reduction products on the growth and activity of the rumen microbial population. British Journal of Nutrition 59, 301–313.
| Effect of nitrate and its reduction products on the growth and activity of the rumen microbial population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhsV2js7Y%3D&md5=ff05a41732de6b2a22aeaf27f41cf507CAS | 3358930PubMed |
Martin AK, Blaxter KL (1965) The energy cost of urea systhesis in sheep. In ‘Energy metabolism’. (Ed. KL Blaxter) pp. 83–91. (Academic Press: London)
Moreno-Vivian C, Cabello P, Martinez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. Journal of Bacteriology 181, 6573–6584.
Newbold JR, van Zijderveld SM, Hulshof RBA, Fokkink WB, Leng RA, Terencio P, Powers WJ, van Adrichem PSJ, Paton ND, Perdok HB (2014) The effect of incremental levels of dietary nitrate on methane emissions in Holstein steers and performance in Nelore bulls. Journal of Animal Science 92, 5032–5040.
| The effect of incremental levels of dietary nitrate on methane emissions in Holstein steers and performance in Nelore bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXisFWis7Y%3D&md5=9e964395af6d2ee6cbe1900e80e25202CAS | 25349351PubMed |
Nolan JV, Hegarty RS, Hegarty J, Godwin IR, Woodgate R (2010) Effects of dietary nitrate on fermentation, methane production and digesta kinetics in sheep. Animal Production Science 50, 801–806.
| Effects of dietary nitrate on fermentation, methane production and digesta kinetics in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrtbzP&md5=c4b3aedbbbfca9ab9c48f4b4570cd5d9CAS |
Onaga T, Nagashima C, Sakata T (2000) Effect of nitric oxide synthase inhibitors on the temporal coordination of duodenal contractions and pancreatic exocrine secretion in sheep. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 170, 469–479.
| Effect of nitric oxide synthase inhibitors on the temporal coordination of duodenal contractions and pancreatic exocrine secretion in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvVKrtrs%3D&md5=e78f6384db092d8bcf94494b5cbfab05CAS | 11083530PubMed |
Onaga T, Okada H, Hagiwara S, Nagashima C, Inoue H, Korczynski W, Kato S (2001) Effects of nitric oxide donor and nitric oxide synthase inhibitor on ruminal contractions in conscious sheep. Research in Veterinary Science 71, 189–195.
| Effects of nitric oxide donor and nitric oxide synthase inhibitor on ruminal contractions in conscious sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1WksLg%3D&md5=de8fd510c05166ad2c6b068c6f632ae0CAS | 11798293PubMed |
Petersen SO, Hellwing ALF, Brask M, Højberg O, Poulsen M, Zhub Z, Khagendra R, Baral KR, Lund P (2015) Dietary nitrate for methane mitigation leads to nitrous oxide emissions from dairy cows. Journal of Environmental Quality 44, 1063–1070.
| Dietary nitrate for methane mitigation leads to nitrous oxide emissions from dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlSnsr%2FP&md5=0cc0a0e603389f4948d63257faac5dd1CAS | 26437087PubMed |
Pfander WH, Ellis WC, Garner GB, Muhrer ME (1956) The absorption of glucose, lactic acid, potassium nitrate, potassium nitrite from the rumen of mature wethers. Journal of Animal Science 15, 1292
Rehberger TG, Hibberd CA (2000) ‘Bacterial composition to reduce the toxic effects of high nitrate consumption in livestock.’ Available at https://www.google.com/patents/US6120810 [Verified 16 March 2016]
Sar C, Mwenya B, Pen B, Takaura K, Morikawa R, Tsujimoto A, Kuwaki K, Isogai N, Shinzato I, Asakura Y, Toride Y, Takahashi J (2005) Effect of ruminal administration of Escherichia coli wild type or a genetically modified strain with enhanced high nitrite reductase activity on methane emission and nitrate toxicity in nitrate-infused sheep. British Journal of Nutrition 94, 691–697.
| Effect of ruminal administration of Escherichia coli wild type or a genetically modified strain with enhanced high nitrite reductase activity on methane emission and nitrate toxicity in nitrate-infused sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1yksrzM&md5=e15a00e9b9c4aaa6acaa1942d89dd279CAS | 16277770PubMed |
Scala G, Maruccio L (2012) Reticular groove of the domestic ruminants: histochemical and immunocytochemical study. Anatomia, Histologia, Embryologia 41, 428–435.
| Reticular groove of the domestic ruminants: histochemical and immunocytochemical study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rlsVWhsQ%3D%3D&md5=7e70bd9f1073bf5738b21eef0797c7aaCAS | 22506730PubMed |
Seerley RW, Emerick RJ, Embry LB, Olsoin OE (1965) Effect of nitrate or nitrite administered continuously in drinking water for swine amd sheep. Journal of Animal Science 24, 1014–1019.
Setchell BP, Williams AJ (1962) Plasma nitrate and nitrite concentration in chronic and acute nitrate poisoning in sheep. Australian Veterinary Journal 38, 58–62.
| Plasma nitrate and nitrite concentration in chronic and acute nitrate poisoning in sheep.Crossref | GoogleScholarGoogle Scholar |
Sharp R, Ziemer CJ, Stern MD, Stahl DA (1998) Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system. FEMS Microbiology Ecology 26, 71–78.
| Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFalsLk%3D&md5=9cf3ce5e62d8acae308f0a6a1885f79aCAS |
Simon J, Eichler R, Pisa R, Biel S, Gross R (2002) Modification of heme c binding motifs in the small subunit (NrfH) of the Wolinella succinogenes cytochrome c nitrite reductase complex. FEBS Letters 522, 83–87.
| Modification of heme c binding motifs in the small subunit (NrfH) of the Wolinella succinogenes cytochrome c nitrite reductase complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFGqsLY%3D&md5=0d60974c7b57cce756a3d591a860b962CAS | 12095623PubMed |
Sinclair KB, Jones DIH (1964) Nitrate toxicity in sheep. Journal of the Science of Food and Agriculture 15, 717–721.
| Nitrate toxicity in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXjt1GrsQ%3D%3D&md5=49407c615097583d0470e456ef3b4dc8CAS |
Soupene E, Lee H, Kustu S (2002) Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally. Proceedings of the National Academy of Sciences of the United States of America 99, 3926–3931.
| Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1Kltbc%3D&md5=65534d7f8bc264519c98175f65944a14CAS | 11891327PubMed |
Stewart V, Parales J (1988) Identification and expression of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12. Journal of Bacteriology 170, 1589–1597.
Stickland LH (1931) The reduction of nitrates by Bact. coli. The Biochemical Journal 25, 1543–1554.
| The reduction of nitrates by Bact. coli.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zjsVynsg%3D%3D&md5=27b619fcbb930b9424584f2437fe6650CAS | 16744721PubMed |
Takaya N (2002) Dissimilatory nitrate reduction metabolisms and their control in fungi. Journal of Bioscience and Bioengineering 94, 506–510.
| Dissimilatory nitrate reduction metabolisms and their control in fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVOns7Y%3D&md5=6fc9cadaa48274763e2b0974534fbe8aCAS | 16233342PubMed |
Tillman AD, Sheriha GM, Sirny RJ (1965) Nitrate reduction studies with sheep. Journal of Animal Science 24, 1140–1146.
Toda N, Okamura T (2003) The pharmacology of nitric oxide in the peripheral nervous system of blood vessels. Pharmacological Reviews 55, 271–324.
| The pharmacology of nitric oxide in the peripheral nervous system of blood vessels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVSgtbY%3D&md5=9dad2f567d9a3b53bc9c6ff2231ff779CAS | 12773630PubMed |
Tsuchiya K, Yoshizumi M, Houchi H, Mason RP (2000) Nitric oxide-forming reaction between the iron-N-methyl-D-glucamine dithiocarbamate complex and nitrite. The Journal of Biological Chemistry 275, 1551–1556.
| Nitric oxide-forming reaction between the iron-N-methyl-D-glucamine dithiocarbamate complex and nitrite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotFWmsg%3D%3D&md5=4af7dfe8fbad0b5733c5eb9f29c4950aCAS | 10636843PubMed |
Tugtas AE, Pavlostathis SG (2007) Inhibitory effects of nitrogen oxides on a mixed methanogenic culture. Biotechnology and Bioengineering 96, 444–455.
| Inhibitory effects of nitrogen oxides on a mixed methanogenic culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVajt7c%3D&md5=4df6ce87b55a4a53033dfdac9ebf7fafCAS | 16865733PubMed |
van Kessel JS, Russell JB (1996) The effect of pH on ruminal methanogenesis. FEMS Microbiology Ecology 20, 205–210.
| The effect of pH on ruminal methanogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkslGiur4%3D&md5=98d6165300bb1728873629b1d1b6bfb8CAS |
van Zijderveld SM (2011) Dietary strategies to reduce methane emissions from ruminants. PhD Thesis, Wageningen University, The Netherlands.
van Zijderveld SM, Gerrits WJ, Apajalahti JA, Newbold JR, Dijkstra J, Leng RA, Perdok HB (2010) Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. Journal of Dairy Science 93, 5856–5866.
| Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1Kis7Y%3D&md5=c84de18e60e1d808cc7a5d43ed5f5cd6CAS | 21094759PubMed |
Veneman JB, Wilkinson TJ, Rubino F, Pinloche E, Hart KJ, Muetzel S, Newbold CJ (2014) ‘Shifts in rumen bacterial population of dairy cows fed two potential methane mitigating additives.’ (INRA-Rowett: Aberdeen, Scotland)
Veneman JB, Muetzel S, Hart KJ, Faulkner CL, Moorby JM, Perdok HB, Newbold CJ (2015) Does dietary mitigation of enteric methane production affect rumen function and animal productivity in dairy cows? PLoS One 10, e0140282
| Does dietary mitigation of enteric methane production affect rumen function and animal productivity in dairy cows?Crossref | GoogleScholarGoogle Scholar | 26509835PubMed |
Vermeiren J, Van de Wiele T, Verstraete W, Boeckx P, Boon N (2009) Nitric oxide production by the human intestinal microbiota by dissimilatory nitrate reduction to ammonium. Journal of Biomedicine & Biotechnology 2009, 284718
| Nitric oxide production by the human intestinal microbiota by dissimilatory nitrate reduction to ammonium.Crossref | GoogleScholarGoogle Scholar |
Wang LC, Garcia-Riveria J, Burris RH (1961) Metabolism of nitrate by cattle. The Biochemical Journal 81, 237–242.
| Metabolism of nitrate by cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XjsVaqsQ%3D%3D&md5=367621b98bf758173339ecebfee555faCAS | 14004854PubMed |
Whatman S, Godwin IR, Nolan JV (2013) Nitrite toxicity in sheep: hypotension or methaemoglobinaemia? Recent Advances in Animal Nutrition in Australia 19, 33–34.
Woods DD (1938) The reduction of nitrate to ammonia by Clostridium welchii. The Biochemical Journal 32, 2000–2012.
| The reduction of nitrate to ammonia by Clostridium welchii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA1MXitlOqtw%3D%3D&md5=56fbeb6e5fa48c112b04a4e66ccc37ecCAS | 16746839PubMed |
Würmli R, Wolffram S, Scharrer E (1987) Inhibition of chloride absorption from the sheep rumen by nitrate. Journal of Veterinary Medicine Series A 34, 476–479.
| Inhibition of chloride absorption from the sheep rumen by nitrate.Crossref | GoogleScholarGoogle Scholar | 3113132PubMed |
Yoshida J, Nakamura Y, Nakamura R (1982) Effects of protozoal fraction and lactate on nitrate metabolism of microorganisms in sheep rumen. Nihon Chikusan Gakkaiho 53, 677–685.
| Effects of protozoal fraction and lactate on nitrate metabolism of microorganisms in sheep rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsFyhtQ%3D%3D&md5=7bb45cc42342e47f377798c7ec94c3daCAS |