Skip to main content
Log in

Mitochondrial haplotype divergences affect specific temperature sensitivity of mitochondrial respiration

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the effect of temperature changes on the functional properties of mitochondria from two sets of D. simulans fly lines harboring the siII and siIII haplotypes in a common nuclear genetic background. We studied four introgressed isofemale lines possessing the mtDNA of siII and the nuclear background of siIII (siII-introgressed) and four lines possessing siIII mitochondria with its native nuclear genome (siIII-controls). We assessed the catalytic capacities of electron transport system (ETS) at four different temperatures (12, 18, 24 and 28 ºC). The impact of temperature on the pyruvate dehydrogenase (PDH) activity, the mitochondrial respiration (coupled and uncoupled respiration), cytochrome c oxidase activity, as well as the excess capacity of complex IV (COX) were evaluated in these two sets of flies. Our results showed that the temperature coefficient values (Q10) measured for mitochondrial respiration in the lower range of temperatures (12 to 18 ºC) showed a 2 to 3 fold increase in siII-introgressed when compared to siIII-controls. This result shows that the impact of temperature on mitochondrial function is different between the two mitotypes studied. The Q10 results seem to be linked to the apparent COX excess capacity of 193 % for siIII-controls that is inexistent for siII-introgressed at 12 ºC. One explanation for these results is that the mitochondria can compensate for the disruption of mito-nuclear interactions at 24 ºC but not at lower temperatures. An alternate explanation would be that siII haplotype confer divergent kinetic properties to the ETS that translate to different temperature sensitivities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ballard JWO (2000a) Comparative genomics of mitochondrial DNA in members of the Drosophila melanogaster subgroup. J Mol Evol 51:48–63

    CAS  Google Scholar 

  • Ballard JWO (2000b) When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol Biol Evol 17:1126–1130

    Article  CAS  Google Scholar 

  • Ballard JWO (2004) Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol Biol Evol 21(3):428–442

    Article  CAS  Google Scholar 

  • Ballard JWO (2005) Drosophila simulans as a novel model for studying mitochondrial metabolism and aging. Exp Gerontol 40:763–773

    Article  CAS  Google Scholar 

  • Ballard JWO, Melvin RG (2010) Linking the mitochondrial genotype to the organismal phenotype. Mol Ecol 19:1523–1539

    Article  CAS  Google Scholar 

  • Ballard JWO, Melvin RG, Katewa SD, Maas K (2007) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution 61:1735–1747

    Article  CAS  Google Scholar 

  • Benard G, Balance N, Jose C, Melser S, Nouette-Gaulain K, Rossignol R (2010) Multi-site control and regulation of mitochondrial energy production. Biochem Biophys Acta 1797:698–709

    Article  CAS  Google Scholar 

  • Blier PU, Guderley HE (1993a) Effects of pH and temperature on the kinetics of pyruvate oxidation by muscle mitochondria from Rainbow Trout (Oncorhynchus mykiss). Physiol Zool 66(4):474–489

    CAS  Google Scholar 

  • Blier PU, Guderley HE (1993b) Mitochondrial activity in rainbow trout red muscle: the effect of temperature on the ADP-dependence of ATP synthesis. J Exp Biol 176:145–158

    CAS  Google Scholar 

  • Blier PU, Lemieux H (2001) The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Artic charr red muscle mitochondria. Comp Biochem Physiol B Biochem Mol Biol 171:247–253

    CAS  Google Scholar 

  • Blier PU, Dufresne F, Burton RS (2001) Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet 17(7):400–406

    Article  CAS  Google Scholar 

  • Das J (2006) The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays 28:890–901

    Article  CAS  Google Scholar 

  • Dean MD, Ballard KJ, Glass A, Ballard JWO (2003) Influence of two Wolbachia strains on population structure of east African Drosophila simulans. Genetics 65:1959–1969

    Google Scholar 

  • Dermitzakis ET, Masly JP, Waldrip HM, Clark AG (2000) Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics 154(2):687–694

    CAS  Google Scholar 

  • Ellison CK, Burton RS (2006) Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus. Evolution 60(7):1382–1391

    CAS  Google Scholar 

  • Fontanillas P, Depraz A, Giorgi MS, Perrin N (2005) Nonshivering thermogenesis capacity associated to mitochondrial DNA haplotypes and gender in the greater white-toothed shrew, Crocidura russula. Mol Ecol 14:661–670

    Article  CAS  Google Scholar 

  • Gnaiger E (2009) Capacity of oxidative phosphorylation in human skeletal muscle: New perspectives of mitochondrial physiology. Int J Biochem Cell Biol 41:1837–1845

    Article  CAS  Google Scholar 

  • Gnaiger E, Lassnig B, Kuznetsov A, Reiger G, Margreiter R (1998) Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J Exp Biol 201:1129–1139

    CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Hood DA, Irrcher I, Ljubicic V, Joseph AM (2006) Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209:2265–2275

    Article  CAS  Google Scholar 

  • James AC, Ballard JWO (2000) Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evolution 54:1661–1672

    CAS  Google Scholar 

  • Katewa SD, Ballard JWO (2007) Sympatric Drosophila simulans flies with distinct mtDNA show difference in mitochondrial respiration and electron transport. Insect Biochem Mol Biol 37:213–222

    Article  CAS  Google Scholar 

  • Kondo R, Satta Y, Matsuura ET, Ishiwa H, Takahata N, Chigusa SI (1990) Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126:657–663

    CAS  Google Scholar 

  • Kunz WS, Kudin A, Vielhaber S, Elger CE, Attardi G, Villani G (2000) Flux control of cytochrome c oxidase in human skeletal muscle. J Biol Chem 274:27741–27745

    Google Scholar 

  • Lemieux H, Tardif J-C, Blier PU (2010) Thermal sensitivity of oxidative phosphorylation in rat heart mitochondria: does pyruvate dehydrogenase dictate the response to temperature? J Therm Biol 35(2):105–111

    Article  CAS  Google Scholar 

  • LeMoine CMR, Genge CE, Moyes CD (2008) Role of the PGC-1 family in the metabolic adaptation of goldfish to diet and temperature. J Exp Biol 211:1448–1455

    Article  CAS  Google Scholar 

  • Letellier T, Malgat M, Coquet M, Moretto B, Parrot-Roulaud F, Mazat J-P (1992) Mitochondrial myopathy studies on permeabilized muscle fibers. Pediatr Res 32:17–22

    Article  CAS  Google Scholar 

  • Letellier T, Heinrich R, Malgat M, Mazat J-P (1994) The kinetic basis of threshold effects observed in mitochondrial diseases: a systemic approach. Biochem J 302:171–174

    CAS  Google Scholar 

  • Liang H, Ward WF (2006) PGC-1 alpha: a key regulator of energy metabolism. Adv Physiol Educ 30:145–151

    Article  Google Scholar 

  • Melvin RG, Katewa SD, Ballard JWO (2008) A candidate complex approach to study functional mitochondrial DNA changes: sequence variation and quaternary structure modeling of Drosophila simulans cytochrome c oxidase. J Mol Evol 66:232–242

    Article  CAS  Google Scholar 

  • Pichaud N, Hébert Chatelain E, Ballard JWO, Tanguay R, Morrow G, Blier PU (2010) Thermal sensitivity of mitochondrial metabolism in two distinct mitotypes of Drosophila simulans: evaluation of mitochondrial plasticity. J Exp Biol 213:1665–1675

    Article  CAS  Google Scholar 

  • Pichaud N, Ballard JWO, Tanguay RM, Blier PU et al (2011) Thermal sensitivity of mitochondrial functions in permeabilized muscle fibers from two populations of Drosophila simulans with divergent mitotypes. Am J Physiol Regul Integr Comp Physiol 30(1)

  • Pichaud N, Ballard JWO, Tanguay RM, Blier PU (2012) Naturally occurring mitochondrial DNA haplotypes exhibit metabolic differences: insight into functional properties of mitochondria. Evolution. doi:10.1111/j.1558-5646.2012.01683.x

  • Puigserver P, Spiegelman BM (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 24:78–90

    Article  CAS  Google Scholar 

  • Rasmussen HN, Rasmussen UF (2003) Oxygen solubilities of media used on electrochemical respiration measurements. Anal Biochem 319:105–113

    Article  CAS  Google Scholar 

  • Rossignol R, Faustin B, Rocher C, Malgat M, Mazat J-P, Letellier T (2003) Mitochondrial threshold effects. Biochem J 370:751–762

    Article  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD et al (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150(76–85):1985

    Google Scholar 

  • Thibeault M, Blier PU, Guderley H (1997) Seasonal variation of muscle metabolic organization in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 16(2):139–155

    Article  Google Scholar 

  • Veksler VI, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA (1987) Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochemica and Biophysica Acta 892:191–196

    Article  CAS  Google Scholar 

  • Villani G, Attardi G (1997) In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc Nat Acad Sci USA 94:1166–1171

    Article  CAS  Google Scholar 

  • Villani G, Greco M, Papa S, Attardi G (1998) Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J Biol Chem 273(48):31829–31836

    Article  CAS  Google Scholar 

  • Willett CS, Burton RS (2004) Evolution of interacting proteins in the mitochondrial electron transport system in a marine copepod. Mol Biol Evol 21(3):443–453

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pierre U. Blier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pichaud, N., Ballard, J.W.O., Tanguay, R.M. et al. Mitochondrial haplotype divergences affect specific temperature sensitivity of mitochondrial respiration. J Bioenerg Biomembr 45, 25–35 (2013). https://doi.org/10.1007/s10863-012-9473-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-012-9473-9

Keywords

Navigation