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Mitochondrial abundance and function in skeletal muscle and liver from Simmental beef cattle divergent for residual feed intake

Published online by Cambridge University Press:  16 March 2020

C. McKenna Open the ORCID record for C. McKenna [Opens in a new window] ,
R. K. Porter ,
C. Fitzsimons ,
S. M. Waters ,
M. McGee  and
D. A. Kenny
C. McKenna
Affiliation:
Animal and Bioscience Department, Animal and Grassland Research and Innovation Centre, Teagasc Grange, Dunsany, County MeathC15 PW93, Ireland School of Biochemistry & Immunology, Trinity College Dublin, Dublin 2D02 R590, Ireland
R. K. Porter
Affiliation:
School of Biochemistry & Immunology, Trinity College Dublin, Dublin 2D02 R590, Ireland
C. Fitzsimons
Affiliation:
Animal and Bioscience Department, Animal and Grassland Research and Innovation Centre, Teagasc Grange, Dunsany, County MeathC15 PW93, Ireland
S. M. Waters
Affiliation:
Animal and Bioscience Department, Animal and Grassland Research and Innovation Centre, Teagasc Grange, Dunsany, County MeathC15 PW93, Ireland
M. McGee
Affiliation:
Animal and Bioscience Department, Animal and Grassland Research and Innovation Centre, Teagasc Grange, Dunsany, County MeathC15 PW93, Ireland
D. A. Kenny*
Affiliation:
Animal and Bioscience Department, Animal and Grassland Research and Innovation Centre, Teagasc Grange, Dunsany, County MeathC15 PW93, Ireland
*
†E-mail: [email protected]
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Abstract

Cellular mitochondrial function has been suggested to contribute to variation in feed efficiency (FE) among animals. The objective of this study was to determine mitochondrial abundance and activities of various mitochondrial respiratory chain complexes (complex I (CI) to complex IV (CIV)) in liver and muscle tissue from beef cattle phenotypically divergent for residual feed intake (RFI), a measure of FE. Individual DM intake (DMI) and growth were measured in purebred Simmental heifers (n = 24) and bulls (n = 28) with an initial mean BW (SD) of 372 kg (39.6) and 387 kg (50.6), respectively. All animals were offered concentrates ad libitum and 3 kg of grass silage daily, and feed intake was recorded for 70 days. Residuals of the regression of DMI on average daily gain (ADG), mid-test BW0.75 and backfat (BF), using all animals, were used to compute individual RFI coefficients. Animals were ranked within sex, by RFI into high (inefficient; top third of the population), medium (middle third of population) and low (efficient; bottom third of the population) terciles. Statistical analysis was carried out using the MIXED procedure of SAS v 9.3. Overall mean ADG (SD) and daily DMI (SD) for heifers were 1.2 (0.4) and 9.1 (0.5) kg, respectively, and for bulls were 1.8 (0.3) and 9.5 (1.02) kg, respectively. Heifers and bulls ranked as high RFI consumed 10% and 15% more (P < 0.05), respectively, than their low RFI counterparts. There was no effect of RFI on mitochondrial abundance in either liver or muscle (P > 0.05). An RFI × sex interaction was apparent for CI activity in muscle. High RFI animals had an increased activity (P < 0.05) of CIV in liver tissue compared to their low RFI counterparts; however, the relevance of that observation is not clear. Our data provide no clear evidence that cellular mitochondrial function within either skeletal muscle or hepatic tissue has an appreciable contributory role to overall variation in FE among beef cattle.

Keywords

feed efficiencygenderoxidative phosphorylationcitrate synthasebovine
Type
Research Article
Information
animal , Volume 14 , Issue 8 , August 2020 , pp. 1710 - 1717
Copyright
© The Animal Consortium 2020

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References

Arthur, PF, Archer, JA, Johnston, DJ, Herd, RM, Richardson, EC and Parnell, PF 2001. Genetic and phenotypic variance and covariance components for feed intake, feed efficiency, and other postweaning traits in Angus cattle. Journal of Animal Science 79, 2805–2811.CrossRefGoogle ScholarPubMed
Basarab, JA, McCartney, D, Okine, EK and Baron, VS 2007. Relationships between progeny residual feed intake and dam productivity traits. Canadian Journal of Animal Science 87, 489–502.CrossRefGoogle Scholar
Basarab, JA, Price, MA, Aalhus, JL, Okine, EK, Snelling, WM and Lyle, KL 2003. Residual feed intake and body composition in young growing cattle. Canadian Journal of Animal Science 83, 189–204.CrossRefGoogle Scholar
Berg, J, Tymozko, J, Gatto, G and Stryer, L 2002. Oxidative phosphorylation. In Biochemistry (ed. Schultz, L and Pech, I), 5th edition, pp. 306–407. W.H. Freeman & Company, New York, NY, USA.Google Scholar
Berry, DP and Crowley, JJ 2013. Cell biology symposium: genetics of feed efficiency in dairy and beef cattle. Journal of Animal Science 91, 1594–1613.CrossRefGoogle ScholarPubMed
Bottje, WG and Kong, BW 2013. Cell Biology Symposium: feed efficiency: mitochondrial function to global gene expression. Journal of Animal Science 91, 1582–1593.CrossRefGoogle ScholarPubMed
Bottje, WG, Khatri, B, Shouse, SA, Seo, D, Mallmann, B, Orlowski, SK, Pan, J, Kong, S, Owens, CM, Anthony, NB and Kim, JK 2017. Identification and differential abundance of mitochondrial genome encoding small RNAs (mitosRNA) in breast muscles of modern broilers and unselected chicken breed. Frontiers in Physiology 8, 816.CrossRefGoogle ScholarPubMed
Bureš, D and Bartoň, L 2012. Growth performance, carcass traits and meat quality of bulls and heifers slaughtered at different ages. Czech Journal of Animal Science 57, 34–43.CrossRefGoogle Scholar
Byrne, CJ, Fair, S, English, AM, Johnston, D, Lonergan, P and Kenny, DA 2017. Effect of milk replacer and concentrate intake on growth rate, feeding behaviour and systemic metabolite concentrations of pre-weaned bull calves of two dairy breeds. Animal 11, 1531–1538.CrossRefGoogle ScholarPubMed
Crews, DH, Lowerison, JM, Caron, N and Kemp, RA 2004. Genetic parameters among growth and carcass traits of Canadian Charolais cattle. Canadian Journal of Animal Science 84, 589–597.CrossRefGoogle Scholar
Crowley, JJ, McGee, M, Kenny, DA, Crews, Jr, DH, Evans, RD and Berry, DP 2010. Phenotypic and genetic parameters for different measures of feed efficiency in different breeds of Irish performance-tested beef bulls. Journal of Animal Science 88, 885–894.CrossRefGoogle ScholarPubMed
Díaz, F, Barrientos, A and Fontanesi, F 2009. Evaluation of the mitochondrial respiratory chain and oxidative phosphorylation system using blue native gel electrophoresis. Current Protocols in Human Genetics. Chapter 19, Unit 19.4.CrossRefGoogle ScholarPubMed
Else, AJ, Barnes, SJ, Danson, MJ and Weitzman, PD 1988. A new spectrophotometric assay for citrate synthase and its use to assess the inhibitory effects of palmitoyl thioesters. Biochemical Journal 251, 803–807.CrossRefGoogle ScholarPubMed
Fitzsimons, C, Kenny, DA, Deighton, MH, Fahey, AG and McGee, M 2013. Methane emissions, body composition, and rumen fermentation traits of beef heifers differing in residual feed intake. Journal of Animal Science 91, 5789–5800.CrossRefGoogle ScholarPubMed
Fitzsimons, C, Kenny, DA, Fahey, AG and McGee, M 2014a. Feeding behavior, ruminal fermentation, and performance of pregnant beef cows differing in phenotypic residual feed intake offered grass silage. Journal of Animal Science 92, 2170–2181.CrossRefGoogle ScholarPubMed
Fitzsimons, C, Kenny, DA and McGee, M 2014b. Visceral organ weights, digestion and carcass characteristics of beef bulls differing in residual feed intake offered a high concentrate diet. Animal 8, 949–959.CrossRefGoogle ScholarPubMed
Fitzsimons, C, McGee, M, Waters, SM and Kenny, DA 2017. Molecular physiology of feed efficiency in beef cattle. In Biology of domestic animals (ed. Scanes, CG and Hill, RA), pp. 122–165. CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
Forbes, JM 2007. Voluntary food intake and diet selection in farm animals, 2nd edition. Cabi, Boston, MA, USACrossRefGoogle Scholar
Gomes, RC, Sainz, RD, Silva, SL, César, MC, Bonin, MN and Leme, PR 2012. Feedlot performance, feed efficiency reranking, carcass traits, body composition, energy requirements, meat quality and calpain system activity in Nellore steers with low and high residual feed intake. Livestock Science 150, 265–273.CrossRefGoogle Scholar
Herd, RM and Arthur, PF 2009. Physiological basis for residual feed intake. Journal of Animal Science 87, E64–E71.CrossRefGoogle ScholarPubMed
Hill, RA and Ahola, JK 2012. Feed efficiency interactions with other traits: growth and product quality. In Feed efficiency in the beef industry (ed. Hill, RA), pp. 145–158. John Wiley and Sons, Hoboken, NJ, USA.CrossRefGoogle Scholar
Iqbal, M, Pumford, NR, Tang, ZX, Lassiter, K, Ojano-Dirain, C, Wing, T, Cooper, M and Bottje, WG 2005. Compromised liver mitochondrial function and complex activity in low feed efficient broilers are associated with higher oxidative stress and differential protein expression. Poultry Science 84, 933–941.CrossRefGoogle ScholarPubMed
Iqbal, M, Pumford, NR, Tang, ZX, Lassiter, K, Wing, T, Cooper, M and Bottje, W 2004. Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poultry Science 83, 474–484.CrossRefGoogle ScholarPubMed
Kelly, AK, Waters, SM, McGee, M, Fonseca, RG, Carberry, C and Kenny, DA 2011. mRNA expression of genes regulating oxidative phosphorylation in the muscle of beef cattle divergently ranked on residual feed intake. Physiological Genomics 43, 12–23.CrossRefGoogle ScholarPubMed
Kenny, DA, Fitzsimons, C, Waters, SM and McGee, M 2018. Improving feed efficiency of beef cattle; current state of the art and future challenges. Animal 12, 1815–1826.CrossRefGoogle ScholarPubMed
Koch, RM, Swiger, LA, Chambers, D and Gregory, KE 1963. Efficiency of feed use in beef cattle. Journal of Animal Science 22, 486–494.CrossRefGoogle Scholar
Kolath, WH, Kerley, MS, Golden, JW and Keisler, DH 2006. The relationship between mitochondrial function and residual feed intake in Angus steers. Journal of Animal Science 84, 861–865.CrossRefGoogle ScholarPubMed
McCarthy, SD, Butler, ST, Patton, J, Daly, M, Morris, DG, Kenny, DA, and Waters, SM 2009. Differences in the expression of genes involved in the somatotropic axis in divergent strains of Holstein-Friesian dairy cows during early and mid lactation. Journal of Dairy Science 92, 5229–5238.CrossRefGoogle ScholarPubMed
McDonald, P, Edwards, RA, Greenhalgh, JF and Morgan, CA 2002. Animal nutrition. Pearson Education Limited, Essex, UK.Google Scholar
McKenna, C, Porter, RK, Keogh, K, Waters, S, McGee, M and Kenny, D 2018. Residual feed intake phenotype and gender affect the expression of key genes of the lipogenesis pathway in subcutaneous adipose tissue of beef cattle. Journal of Animal Science and Biotechnology 20, 68.CrossRefGoogle Scholar
Moraes, GF, Abreu, LR, Ferreira, IC and Pereira, IG 2017. Genetic analysis of residual feed intake adjusted for fat and carcass and performance traits in a Nellore herd. Ciência Rural 47, 20151505.CrossRefGoogle Scholar
Niemann, H, Kuhla, B and Flachowsky, G 2011. Perspectives for feed-efficient animal production. Journal of Animal Science 89, 4344–4363.CrossRefGoogle ScholarPubMed
Nkrumah, JD, Crews, Jr, DH, Basarab, JA, Price, MA, Okine, EK, Wang, Z, Li, C and Moore, SS 2007. Genetic and phenotypic relationships of feeding behavior and temperament with performance, feed efficiency, ultrasound, and carcass merit of beef cattle. Journal of Animal Science 85, 2382–2390.CrossRefGoogle ScholarPubMed
Ramos, MH and Kerley, MS 2013. Mitochondrial complex I protein differs among residual feed intake phenotype in beef cattle. Journal of Animal Science 91, 3299–3304.CrossRefGoogle ScholarPubMed
Rooney, MF, Porter, RK, Katz, LM and Hill, EW 2017. Skeletal muscle mitochondrial bioenergetics and associations with myostatin genotypes in the Thoroughbred horse. PLoS ONE 12, e0186247.CrossRefGoogle ScholarPubMed
Sandelin, BA 2005. Association of mitochondrial biochemistry and electron transport chain protein expression with feed efficiency in Angus cattle. PhD thesis, University of Arkansas, Fayetteville, AR, USA.Google Scholar
Šavc, M, Duane, M, O’Grady, LE, Somers, JR and Beltman, ME 2016. Uterine disease and its effect on subsequent reproductive performance of dairy cattle: a comparison of two cow-side diagnostic methods. Theriogenology 86, 1983–1988.CrossRefGoogle ScholarPubMed
Savietto, D, Berry, DP and Friggens, NC 2014. Towards an improved estimation of the biological components of residual feed intake in growing cattle. Journal of Animal Science 92, 467–476.CrossRefGoogle ScholarPubMed
Schwarzer, M 2016. Models to investigate cardiac metabolism. In The scientist’s guide to cardiac metabolism (ed. M Schwarzer, T Doenst), pp. 103–122. Academic Press, Boston, MA, USA.CrossRefGoogle Scholar
Sharifabadi, HR, Zamiri, MJ, Rowghani, E and Bottje, WG 2012. Relationship between the activity of mitochondrial respiratory chain complexes and feed efficiency in fat-tailed Ghezel lambs. Journal of Animal Science 90, 1807–1815.CrossRefGoogle ScholarPubMed
Spinazzi, M, Casarin, A, Pertegato, V, Salviati, L and Angelini, C 2012. Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nature Protocols 7, 1235.CrossRefGoogle ScholarPubMed
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