Characterization of bovine ruminal and equine cecal microbial populations enriched for enhanced nitro-toxin metabolizing activity.
Abstract: The nitrotoxins 3-nitro-1-propionic acid (NPA) and 3-nitro-1-propanol (NPOH) are produced by a wide variety of leguminous plants, including over 150 different species and varieties of Astragalus potentially grazed by livestock. These toxins are known to be detoxified by at least one ruminal bacterium but detoxification by bacteria from other gut habitats is not known. In the present study, mixed populations of bovine ruminal and equine cecal microbes were enriched for NPA-metabolizing bacteria via consecutive 24-72 h culture in a basal minimal rumen fluid-based medium supplemented with 4.2 mM NPA and H₂ as the energy source. Rates of NPA metabolism by the respective populations increased from 58.4 ± 4.8 and 8.6 ± 11.6 nmol NPA/mL per h during initial culture to 88.9 ± 30.6 and 50.2 ± 30.9 nmol NPA/mL per h following enrichment. Results from 3-tube most probable number tests indicated that numbers of NPA-degrading microbes increased 2.1 and 1.8 log₁₀ units during enrichment from numbers measured pre-enrichment (3.9 × 10³ and 4.3 × 10¹ cells/mL for ruminal and equine cecal populations, respectively). Hydrogen, formate, and to a lesser extent, DL-lactic acid, served as electron donors to the enriched populations and CO₂ or formate were needed to maintain high rates of NPA-metabolism. The NPA-enriched populations were able to metabolize nitrate which, being a preferred electron acceptor, was antagonistic to NPA metabolism. Supplemental NPA was inhibitory to methanogenesis. Fermentation balance estimates indicated that only 47.6% of carbon available in potential substrates was recovered in headspace CO₂, volatile fatty acids or unmetabolized NPA after 72 h incubation of NPA-enriched populations that had metabolized 98% of 8.4 mM added NPA. Overall, these results reveal low level carriage of NPA-metabolizing, CO₂ or formate-requiring bacterial populations in the equine cecum yet support the concept that Denitrobacterium detoxificans-like organisms may well be the functional agents of NPA and NPOH detoxification in the populations studied here.
Published by Elsevier Ltd.
Publication Date: 2013-12-27 PubMed ID: 24374155DOI: 10.1016/j.anaerobe.2013.12.001Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This research explores how gut bacteria found in cows and horses interact with and detoxify toxic substances produced by leguminous plants, specifically focusing on toxins called 3-nitro-1-propionic acid (NPA) and 3-nitro-1-propanol (NPOH). The study finds that these gut bacterial populations can be enriched to increase their toxin metabolizing activity, potentially revealing a new understanding of how digestion in these animals takes place.
Objective of the Study
- The aim of the study was to explore the detoxifying capabilities of gut bacteria in cows (bovine ruminal) and horses (equine cecal) towards nitrotoxins, NPA and NPOH. These toxins are naturally found in various leguminous plants consumed by livestock.
Methodology
- The researchers enriched the bovine and equine bacterial populations to enhance their NPA metabolizing activity. This was achieved by keeping them in a culture with NPA and Hydrogen (H₂) as the energy source for a continuous period of 24 to 72 hours.
- The researchers then compared the rate of NPA metabolism before and after enrichment, giving a measure of how the bacteria’s toxin-processing ability had improved.
- They further probed the behavior of these toxin-metabolizing bacteria, evaluating their interaction with various donors and acceptors of electrons, which are crucial in energy production during metabolism.
Results
- The enrichment process resulted in an increase in the rate of NPA metabolism and in the count of NPA-degrading microbes in both the ruminal and equine cecal populations.
- The results suggested that the enriched populations could metabolize nitrate, which is likely to interfere with NPA metabolism as it acts as a preferred electron acceptor.
- Further findings indicated that NPA could inhibit methanogenesis, a critical metabolic process in ruminants, where organic matter is converted into methane by microorganisms.
- However, the research showcased a discrepancy in the recovery of carbon from potential substrates during incubation, indicating incomplete understanding of the metabolic pathways used for NPA degradation.
Significance of the Research
- This research lays the groundwork for a better understanding of the role of gut bacteria in detoxifying plant toxins in ruminants and equine species.
- It also supports the notion that Detoxificans-like organisms might be the functional agents of NPA and NPOH detoxification in the populations studied.
- These findings could have implications for the health and nutrition management of livestock and offering insights into maximizing diet efficiency and minimizing potential toxic exposure for these animals.
Cite This Article
APA
Zhang Y, Long R, Warzecha CM, Coverdale JA, Latham EA, Hume ME, Callaway TR, O'Neil MR, Beier RC, Anderson RC, Nisbet DJ.
(2013).
Characterization of bovine ruminal and equine cecal microbial populations enriched for enhanced nitro-toxin metabolizing activity.
Anaerobe, 26, 7-13.
https://doi.org/10.1016/j.anaerobe.2013.12.001 Publication
Researcher Affiliations
- Tibetan Rangeland and Yak Research Institute, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou City 730020, China; International Centre for Tibetan Plateau Ecosystem Management, Lanzhou University, Lanzhou City 730020, China; United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F&B Road, College Station, TX 77845, USA.
- Tibetan Rangeland and Yak Research Institute, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou City 730020, China; International Centre for Tibetan Plateau Ecosystem Management, Lanzhou University, Lanzhou City 730020, China.
- Department of Animal Science, Texas A&M University, College Station, TX 77843, USA.
- Department of Animal Science, Texas A&M University, College Station, TX 77843, USA.
- Department of Animal Science, Texas A&M University, College Station, TX 77843, USA.
- United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F&B Road, College Station, TX 77845, USA.
- United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F&B Road, College Station, TX 77845, USA.
- Nutritional Physiology Group, Department of Animal Science, Iowa State University, Ames, IA 50011, USA.
- United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F&B Road, College Station, TX 77845, USA.
- United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F&B Road, College Station, TX 77845, USA. Electronic address: robin.anderson@ars.usda.gov.
- United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F&B Road, College Station, TX 77845, USA.
MeSH Terms
- Animals
- Bacteria / isolation & purification
- Bacteria / metabolism
- Biotransformation
- Carbon Dioxide / metabolism
- Cattle
- Cecum / microbiology
- Formates / metabolism
- Horses
- Hydrogen / metabolism
- Lactic Acid / metabolism
- Nitro Compounds / metabolism
- Propanols / metabolism
- Propionates / metabolism
- Rumen / microbiology
Citations
This article has been cited 3 times.- Bénit P, Goncalves J, El Khoury R, Rak M, Favier J, Gimenez-Roqueplo AP, Rustin P. Succinate Dehydrogenase, Succinate, and Superoxides: A Genetic, Epigenetic, Metabolic, Environmental Explosive Crossroad. Biomedicines 2022 Jul 25;10(8).
- Latham EA, Anderson RC, Pinchak WE, Nisbet DJ. Insights on Alterations to the Rumen Ecosystem by Nitrate and Nitrocompounds. Front Microbiol 2016;7:228.
- Guo W, Wang W, Zhang Y, Zhou M. Effect of 3-Nitropropionic Acid at Different Doses on In Vitro Rumen Fermentation, Digestibility, and Methane Emissions of Grazing Yak and Cattle. Animals (Basel) 2024 Jun 17;14(12).
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