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Mitochondrial plasticity in brachiopod (Liothyrella spp.) smooth adductor muscle as a result of season and latitude

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Abstract

Habitat temperature and mitochondrial volume density (Vv(mt,mf)) are negatively correlated in fishes, while seasonal acclimatization may increase Vv(mt,mf) or the surface density of the mitochondrial cristae (Sv(im,mt)). The effect of temperature on invertebrate mitochondria is essentially unknown. A comparison of two articulate brachiopod species, Liothyrella uva collected from Rothera Station, Antarctica in summer 2007, and Liothyrella neozelanica collected from Fiordland, New Zealand in winter 2007 and summer 2008, revealed a higher Vv(mt,mf) in the Antarctic brachiopod. The Sv(im,mt) was, however, significantly lower, indicating the Antarctic brachiopods have more, less reactive mitochondria. L. uva, from the colder environment, had larger adductor muscles in both absolute and relative terms than the temperate L. neozelanica. Furthermore, a seasonal comparison (winter vs. summer) in L. neozelanica showed that the absolute and relative size of the adductor increased in winter, Vv(mt,mf) was unchanged, and Sv(im,mt) was significantly increased. Thus, seasonal acclimatization to the cold resulted in the same number of more reactive mitochondria. L. neozelanica was clearly able to adapt to seasonal changes using a different mechanism, i.e. primarily through regulation of cristae surface area as opposed to mitochondrial volume density. Furthermore, given the evolutionary age of these living fossils (i.e. approximately 550 million years), this suggests that mitochondrial plasticity has roots extending far back into evolutionary history.

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References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol 138A:405–415

    CAS  Google Scholar 

  • Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275:81–86

    CAS  PubMed  Google Scholar 

  • Cornelisen C, Goodwin E (2008) Tailrace discharge from the Manapouri power station and its effects on water temperature in Doubtful Sound, Cawthron Report No. 1543, p 45. Cawthron Institute, Nelson

  • Crockett EL, Sidell BD (1990) Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol Zool 63:472–488

    Google Scholar 

  • Egginton S, Sidell BD (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol 256:R1–R9

    CAS  PubMed  Google Scholar 

  • Ellis EA (2002) New embedding formulations using Quetol 651. Microsc Microanal 8:884–885

    Google Scholar 

  • Goebel NL, Wing SR, Boyd PW (2005) A mechanism for onset of diatom blooms in a fjord with persistent salinity stratification. Estuar Coast Shelf Sci 64:546–560

    Article  Google Scholar 

  • Guderley H (2004a) Locomotor performance and muscle metabolic capacities: impact of temperature and energetic status. Comp Biochem Physiol 139B:371–382

    CAS  Google Scholar 

  • Guderley H (2004b) Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427

    Article  PubMed  Google Scholar 

  • Haugen T, Kiessling A, Olsen RE, Rora MB, Slinde E, Nortvedt R (2006) Seasonal variations in muscle growth dynamics and selected quality attributes in Atlantic halibut (Hippoglossus hippoglossus L.) fed dietary lipids containing soybean and/or herring oil under different rearing regimes. Aquaculutre 261:565–579

    Article  CAS  Google Scholar 

  • Houten SM, Auwerx J (2004) PGC-1α: turbocharging mitochondria. Cell 119:5–7

    Article  CAS  PubMed  Google Scholar 

  • James MA, Ansell AD, Collins MJ, Curry GB, Peck LS, Rhodes MC (1992) Biology of living brachiopods. Adv Mar Biol 28:175–387

    Article  Google Scholar 

  • Johnston IA (1993) Phenotypic plasticity of fish muscle to temperature change. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 322–340

    Google Scholar 

  • Johnston IA, Calvo J, Guderley H, Fernandez D, Palmer L (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12

    CAS  PubMed  Google Scholar 

  • Johnston IA, Fernandez D, Calvo J, Vieira VLA, North AW, Abercromby M, Garland T Jr (2003) Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective. J Exp Biol 206:2595–2609

    Article  PubMed  Google Scholar 

  • Kinsey ST, Hardy KM, Locke BR (2007) The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle. J Exp Biol 210:3505–3512

    Article  CAS  PubMed  Google Scholar 

  • Logue JA, de Vries AL, Fodor E, Cossins AR (2000) Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J Exp Biol 203:2105–2115

    CAS  PubMed  Google Scholar 

  • Moon TW, Hulbert WC (1975) The ultrastructure of the mantle musculature of the squid Symplectoteuthis oualaniensis. Comp Biochem Physiol 52B:145

    Google Scholar 

  • Morley SA, Lurman G, Skepper JN, Pörtner H-O, Peck LS (2009) Thermal plasticity of mitochondria: a latitudinal comparison between Southern Ocean molluscs. Comp Biochem Physiol 152A:423–430

    CAS  Google Scholar 

  • Peck LS (1996) Metabolism and feeding in the antarctic brachiopod Liothyrella uva: a low energy lifestyle species with restricted metabolic scope. Proc R Soc 263B:223–228

    Google Scholar 

  • Peck LS (2001) Ecology of articulated brachiopods. In: Calson S, Sandy S (eds) Brachiopods ancient, modern, vol 7. The Paleontological Society, Kansas, pp 171–184

    Google Scholar 

  • Peck LS, Holmes LJ (1989) Seasonal and ontogenetic changes in tissue size in the Antarctic brachiopod Liothyrella uva (Broderip, 1833). J Exp Mar Biol Ecol 134:25–36

    Article  Google Scholar 

  • Peck LS, Clarke A, Holmes L (1987) Summer metabolism and seasonal biochemical changes in the brachiopod Liothyrella uva (Jackson, 1912). J Exp Mar Biol Ecol 114:85–97

    Article  Google Scholar 

  • Peck LS, Brockington S, Brey T (1997) Growth and metabolism in the Antarctic brachiopod Liothyrella uva. Philos Trans R Soc Lond 352:851–858

    Article  Google Scholar 

  • Peck LS, Barnes DKA, Willmott J (2005) Responses to extreme seasonality in food supply: diet plasticity in Antarctic brachiopods. Mar Biol 147:453–463

    Article  Google Scholar 

  • Philipp EER, Schmidt M, Gsottbauer C, Sänger AM, Abele D (2008) Size- and age-dependent changes in adductor muscle swimming physiology of the scallop Aequipecten opercularis. J Exp Biol 211:2492–2501

    Article  PubMed  Google Scholar 

  • Rhodes MC, Thayer CW (1991) Effects of turbidity on suspension feeding: are brachiopods better then bivalves? In: MacKinnon DI, Lee DE, Campbell JD (eds) Brachiopods though time. Balkema, Rotterdam, pp 191–196

    Google Scholar 

  • Rome LC (1990) Influence of temperature on muscle recruitment and muscle function in vivo. Am J Physiol 259:R210–R222

    CAS  PubMed  Google Scholar 

  • Sänger A (1993) Limits to the acclimation of fish muscle. Rev Fish Biol Fish 3:1–15

    Article  Google Scholar 

  • Sidell BD (1980) Responses of goldfish (Carassius auratus, L.) muscle to temperature acclimation: alterations in biochemistry and proportions of different fiber types. Physiol Zool 53:98–107

    CAS  Google Scholar 

  • Sidell BD, Hazel JR (1987) Temperature affects the diffusion of small molecules through cytosol of fish muscle. J Exp Biol 129:191–203

    CAS  PubMed  Google Scholar 

  • Sidell BD, Moerland TS (1989) Effects of temperature on muscular function and locomotory performance in teleost fish. Adv Comp Env Physiol 5:116–156

    Google Scholar 

  • Sommer AM, Pörtner H-O (2002) Metabolic cold adaptation in the lugworm Arenicola marina: comparison of a North Sea and a White Sea population. Mar Ecol Prog Ser 240:171–182

    Article  Google Scholar 

  • St-Pierre J, Charest PM, Guderley H (1998) Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatisation of rainbow trout Oncorhynchus mykiss. J Exp Biol 201:2961–2970

    CAS  Google Scholar 

  • Urschel MR, O’Brien KM (2008) High mitochondrial densities in the hearts of Antarctic icefishes are maintained by an increase in mitochondrial size rather than mitochondrial biogenesis. J Exp Biol 211:2638–2646

    Article  CAS  PubMed  Google Scholar 

  • Watabe S (2002) Temperature plasticity of contractile proteins in fish muscle. J Exp Biol 205:2231–2236

    CAS  PubMed  Google Scholar 

  • Weibel ER (1979) Stereological methods. Academic, London

    Google Scholar 

Download references

Acknowledgments

Thanks to Mike Barker and Paul Meredith, Stephanie Martin and Melody Clark for help collecting brachiopods in New Zealand. The Rothera dive team, especially the marine assistant who helped in collecting and transporting Antarctic brachiopods. Mike Barker is thanked for the L. neozelanica photo. This project was financed in part by the ESF ThermAdapt short visit grant (2,148) awarded to GL, a Society for Experimental Biology travel grant awarded to GL, the University of Bern. It was also supported by funding from the Natural Environment Research Council via the British Antarctic Survey BIOREACH project in the BIOFLAME programme.

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Correspondence to Glenn J. Lurman.

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Communicated by J. P. Grassle.

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227_2009_1374_MOESM1_ESM.tif

Fig. 2 A) Electron micrograph of adductor muscle from Liothyrella uva. Mitochondria are indicated with arrowheads. Scale bar represents 5 µm. B) Electron micrograph of a single mitochondrion in Liothyrella uva adductor muscle. Scale bar represents 1 µm (TIFF 34020 kb)

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Lurman, G.J., Blaser, T., Lamare, M. et al. Mitochondrial plasticity in brachiopod (Liothyrella spp.) smooth adductor muscle as a result of season and latitude. Mar Biol 157, 907–913 (2010). https://doi.org/10.1007/s00227-009-1374-z

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