Hostname: page-component-848d4c4894-mwx4w Total loading time: 0 Render date: 2024-06-26T15:30:50.543Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of oxalic acid on rumen function and bacterial community in sheep

Published online by Cambridge University Press:  08 January 2013

A. Belenguer ,
M. Ben Bati ,
G. Hervás ,
P. G. Toral ,
D. R. Yáñez-Ruiz  and
P. Frutos
A. Belenguer*
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n, 24346 Grulleros, León, Spain
M. Ben Bati
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n, 24346 Grulleros, León, Spain
G. Hervás
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n, 24346 Grulleros, León, Spain
P. G. Toral
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n, 24346 Grulleros, León, Spain
D. R. Yáñez-Ruiz
Affiliation:
Estación Experimental del Zaidín (CSIC), Profesor Albareda 1, 18008 Granada, Spain
P. Frutos
Affiliation:
Instituto de Ganadería de Montaña (CSIC-ULE), Finca Marzanas s/n, 24346 Grulleros, León, Spain
*
†E-mail: a.belenguer@csic.es
Get access

Abstract

Oxalic acid (OA) is a secondary compound occurring in a wide range of plants consumed by ruminants, especially in saline lands or in arid and semi-arid regions. However, its impact on the rumen microbial community and its changes over time, as well as the potential consequences on ruminal function, remain unknown. To examine this impact, five ewes fitted with a ruminal cannula and fed low-quality grass hay were dosed daily with 0.6 mmol of OA/kg body weight through the cannula for 14 days. On days 0 (before the start), 4, 7 and 14 of the administration period, samples of ruminal digesta were collected throughout the day (0, 3, 6 and 9 h after the morning feeding) for analysis of the bacterial community and fermentation parameters (pH, ammonia and volatile fatty acid (VFA) concentrations). In addition, two feedstuffs were incubated in situ using the nylon bag technique to estimate ruminal degradation. Terminal restriction fragment length polymorphism was employed to monitor the dynamics of total bacteria, and quantitative real-time PCR was used to investigate the abundance of the oxalate-degrading Oxalobacter formigenes. Neither pH nor total VFA concentrations were affected. Nevertheless, OA dosing altered molar proportions of most individual VFA and ammonia concentrations (P < 0.001). The dry matter disappearance of alfalfa hay was reduced on days 7 and 14 and that of barley straw only on day 7 (P < 0.01). These slight changes were related to others observed in the relative frequency of a number of terminal restriction fragments. Variations in the ruminal microbiota occurred rapidly with OA administration, which did not modify the bacterial diversity significantly but altered the structure of the community. However, many of these changes were reversed by the end of the experiment, with no significant differences between days 0 and 14 of dosing. These results suggest a rapid adaptation of the rumen bacterial community linked to the estimated increase in the abundance of O. formigenes (from 0.002% to 0.007% of oxc gene in relation to the total bacteria 16S rDNA; P < 0.01), which is assumed to be responsible for oxalate breakdown.

Keywords

Oxalobacter formigenesoxalatesreal-time PCRruminal microbiotaT-RFLP
Type
Nutrition
Information
animal , Volume 7 , Issue 6 , June 2013 , pp. 940 - 947
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdo, Z, Schüette, UME, Bent, SJ, Williams, CJ, Forney, LJ, Joyce, P 2006. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environmental Microbiology 8, 929–938.Google Scholar
Abratt, VR, Reid, SJ 2010. Oxalate-degrading bacteria of the human gut as probiotics in the management of kidney stone disease. Advances in Applied Microbiology 72, 63–87.CrossRefGoogle Scholar
Agricultural and Food Research Council (AFRC) 1993. Energy and protein requirements of ruminants: an advisory manual prepared by the AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford, UK.Google Scholar
Allison, MJ, Littledike, ET, James, LF 1977. Changes in ruminal oxalate degradation rates associated with adaptation to oxalate ingestion. Journal of Animal Science 45, 1173–1179.Google Scholar
Allison, MJ, Dawson, KA, Mayberry, WR, Foss, JG 1985. Oxalobacter formigenes gen. Nov., sp. Nov.: oxalate-degrading anaerobes that inhabit the gastrointestinal tract. Archives of Microbiology 141, 1–7.Google Scholar
Belenguer, A, Hervás, G, Yañez-Ruiz, DR, Toral, PG, Ezquerro, C, Frutos, P 2010. Preliminary study of the changes in rumen bacterial populations from cattle intoxicated with young oak (Quercus pyrenaica) leaves. Animal Production Science 50, 228–234.Google Scholar
Ben Salem, H, Norman, HC, Nefzaoui, A, Mayberry, DE, Pearce, KL, Revell, DK 2010. Potential use of oldman saltbush (Atriplex mummularia Lindl.) in sheep and goat feeding. Small Ruminant Research 91, 13–28.Google Scholar
Cheeke, PR 1995. Endogenous toxins and mycotoxins in forage grasses and their effects on livestock. Journal of Animal Science 73, 909–918.Google Scholar
Cole, JR, Wang, Q, Cardenas, E, Fish, J, Chai, B, Farris, RJ, Kulam-Syed-Mohideen, AS, McGarrell, DM, Marsh, T, Garrity, GM, Tiedje, JM 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37, D141–D145.CrossRefGoogle ScholarPubMed
Daniel, SL, Cook, HM, Hartman, PA, Allison, MJ 1989. Enumeration of anaerobic oxalate-degrading bacteria in the ruminal contents of sheep. FEMS Microbiology Ecology 62, 329–334.Google Scholar
Dawson, KA, Allison, MJ, Hartman, PA 1980. Isolation and some characteristics of anaerobic oxalate-degrading bacteria from the rumen. Applied and Environmental Microbiology 40, 833–839.Google Scholar
Duncan, AJ, Frutos, P, Young, SA 1997. Rates of oxalic acid degradation in the rumen of sheep and goats in response to different levels of oxalic acid administration. Animal Science 65, 451–456.Google Scholar
Duncan, AJ, Frutos, P, Young, SA 2000. The effect of rumen adaptation to oxalic acid on selection of oxalic acid-rich plants by goats. British Journal of Nutrition 83, 59–65.Google Scholar
Edwards, JE, McEwan, NR, Travis, AJ, Wallace, RJ 2004. 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie van Leeuwenhoek 86, 263–281.CrossRefGoogle Scholar
El Shaer, HM 2010. Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region. Small Ruminant Research 91, 3–12.Google Scholar
Frey, JC, Pell, AN, Berthiaume, R, Lapierre, H, Lee, S, HaJ, K, Mendell, JE, Angert, ER 2009. Comparative studies of microbial populations in the rumen, duodenum, ileum and faeces of lactating dairy cows. Journal of Applied Microbiology 108, 1982–1993.Google Scholar
Frutos, P, Duncan, AJ, Kyriazakis, I, Gordon, IJ 1998. Learned aversion towards oxalic acid-containing foods by goats: does rumen adaptation to oxalic acid influence diet choice? Journal of Chemical Ecology 24, 383–397.Google Scholar
Hartmann, M, Widmer, F 2008. Reliability for detecting composition and changes of microbial communities by T-RFLP genetic profiling. FEMS Microbiology Ecology 63, 249–260.Google Scholar
Hill, TCJ, Walsh, KA, Harris, JA, Moffett, BF 2003. Using ecological diversity measures with bacterial communities. FEMS Microbiology Ecology 43, 1–11.Google Scholar
Hongoh, YH, Yuzawa, M, Okhuma, M, Kudo, T 2003. Evaluation of primers and PCR conditions for the analysis of 16S rRNA genes from a natural environment. FEMS Microbiology Letters 221, 299–304.Google Scholar
James, LF 1972. Oxalate toxicosis. Clinical Toxicology 5, 231–243.CrossRefGoogle ScholarPubMed
Jiang, J, Knight, J, Easter, LH, Neiberg, R, Holmes, RP, Assimos, DG 2011. Impact of dietary calcium and oxalate, and Oxalobacter formigenes colonization on urinary oxalate excretion. Journal of Urology 186, 135–139.Google Scholar
Khammar, N, Martin, G, Ferro, K, Job, D, Aragno, M, Verrecchia, E 2009. Use of the frc gene as a molecular marker to characterize oxalate-oxidizing bacterial abundance and diversity structure in soil. Journal of Microbiology Methods 76, 120–127.Google Scholar
Krause, DO, Russell, JB 1996. An rRNA approach for assessing the role of obligate amino acid-fermenting bacteria in ruminal amino acid deamination. Applied and Environmental Microbiology 62, 815–821.Google Scholar
Krause, DO, Denman, SE, Mackie, RI, Morrison, M, Rae, AL, Attwood, GT, McSweeney, CS 2003. Opportunities to improve fiber degradation in the rumen: microbiology, ecology, and genomics. FEMS Microbiology Reviews 27, 663–693.Google Scholar
Libert, B, Franceschi, VR 1987. Oxalate in crop plants. Journal of Agriculture and Food Chemistry 35, 926–938.Google Scholar
McSweeney, CS, Denman, SE 2007. Effect of sulfur supplements on cellulolytic rumen micro-organisms and microbial protein synthesis in cattle fed a high fibre diet. Journal of Applied Microbiology 103, 1757–1765.Google Scholar
Mertens, DR 2002. Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: collaborative study. Journal of AOAC International 85, 1217–1240.Google Scholar
Mrazek, J, Tepsi, K, Avgustin, G, Kopecny, J 2006. Diet-dependent shifts in ruminal butyrate-producing bacteria. Folia Microbiologica 51, 294–298.Google Scholar
Ottenstein, DM, Bartley, DA 1971. Improved gas chromatography separation of free acids C2–C5 in dilute solution. Analytical Chemistry 43, 952–955.Google Scholar
Rahman, MM, Kawamura, O 2011. Oxalate accumulation in forage plants: some agronomic, climatic and genetic aspects. Asian-Australasian Journal of Animal Science 24, 439–448.Google Scholar
Russell, JB, Wallace, RJ 1997. Energy-yielding and energy-consuming reactions. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 246–282. Chapman and Hall, London, UK.Google Scholar
Sahin, N 2003. Oxalotrophic bacteria. Research in Microbiology 154, 399–407.Google Scholar
Tajima, K, Aminov, RI, Nagamine, T, Matsui, H, Nakamura, M, Benno, Y 2001. Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Applied and Environmental Microbiology 67, 2766–2774.Google Scholar
Wallace, RJ 2008. Gut microbiology – broad genetic diversity, yet specific metabolic niches. Animal 2, 661–668.Google Scholar
Weatherburn, MW 1967. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39, 971–974.Google Scholar