Abstract

Ruminal methane production is among the main targets for greenhouse gas (GHG) mitigation for the animal agriculture industry. Many compounds have been evaluated for their efficacy to suppress enteric methane production by ruminal microorganisms. Of these, nitrate as an alternative hydrogen sink has been among the most promising, but it suffers from variability in efficacy for reasons that are not understood. The accumulation of nitrite, which is poisonous when absorbed into the animal’s circulation, is also variable and poorly understood. This review identifies large gaps in our knowledge of rumen microbial ecology that handicap the further development and safety of nitrate as a dietary additive. Three main bacterial species have been associated historically with ruminal nitrate reduction, namely Wolinella succinogenes, Veillonella parvula, and Selenomonas ruminantium, but others almost certainly exist in the largely uncultivated ruminal microbiota. Indications are strong that ciliate protozoa can reduce nitrate, but the significance of their role relative to bacteria is not known. The metabolic fate of the reduced nitrate has not been studied in detail. It is important to be sure that nitrate metabolism and efforts to enhance rates of nitrite reduction do not lead to the evolution of the much more potent GHG, nitrous oxide. The relative importance of direct inhibition of archaeal methanogenic enzymes by nitrite or the efficiency of capture of hydrogen by nitrate reduction in lowering methane production is also not known, nor are nitrite effects on other members of the microbiota. How effective would combining mitigation methods be, based on our understanding of the effects of nitrate and nitrite on the microbiome? Answering these fundamental microbiological questions is essential in assessing the potential of dietary nitrate to limit methane emissions from ruminant livestock.

Highlights

  • Until relatively recently, the main driver for research on ruminal nitrate metabolism was nitrate poisoning and nitrite toxicity

  • The results have been among the most promising of all the interventions investigated to date (Hristov et al, 2013a), yet variations in response, e.g., in relation to the basal diet (Troy et al, 2015), are difficult to explain, in microbiological terms. Another property in favor of nitrate as a feed additive is that it can have nutritional benefits associated with protein nutrition additional to those deriving from lower methane emissions

  • It could be speculated that nitrite, rather than nitrate, might be a better compound to use to induce this adaptation, because nitrate itself will enrich for enhanced nitrate reduction as well, but we were unable to find any published evidence of nitrite having been used in this way

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Summary

INTRODUCTION

The main driver for research on ruminal nitrate metabolism was nitrate poisoning and nitrite toxicity. The results of Iwamoto et al (1999, 2001a) with goat ruminal digesta indicated the same, though the authors found toxicity to the microbes as measured by lower volatile fatty acid (VFA) production These findings were instrumental in stimulating in vivo experiments to evaluate the usefulness of nitrate as a methanogenesis-inhibiting feed additive/ingredient. The results have been among the most promising of all the interventions investigated to date (Hristov et al, 2013a), yet variations in response, e.g., in relation to the basal diet (Troy et al, 2015), are difficult to explain (see the excellent review by Lee and Beauchemin, 2014), in microbiological terms Another property in favor of nitrate as a feed additive is that it can have nutritional benefits associated with protein nutrition additional to those deriving from lower methane emissions. It should be noted that this does not apply to situations for example where temperate forages are grazed and in which N supply to the rumen is in excess; in this situation, use of nitrate would lower the efficiency of N utilization

NITRATE METABOLISM IN THE RUMEN AND NITRITE TOXICITY
MICROBIAL SPECIES INVOLVED IN METHANOGENESIS AND NITRATE REDUCTION
Ciliate Protozoa
MECHANISMS OF INHIBITION OF METHANOGENESIS BY NITRATE
Anaerobic Fungi
IMPACT OF NITRATE ON OTHER METABOLIC ACTIVITIES OF THE RUMINAL MICROBIOTA
IMPROVING THE SAFETY AND EFFICACY OF NITRATE SUPPLEMENTATION
Findings
LIKELY CONSEQUENCES OF INHIBITING METHANOGENESIS ON PRODUCTIVITY
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