Summary
Through computer simulation of images produced by the transmission electron microscope (TEM), we have identified three-dimensional periodic cubic membrane structures in giant amoebae ( Chaos carolinensis) mitochondria. The cubic membranes are based on the highly curved three-dimensional periodic cubic surfaces, sharing the same geometry of mathematically defined periodic minimal surfaces. The double-membrane structures identified here divide space into three separate and convoluted subspaces. Specimen preparation, specifically the tendency to cut oblique sections, of this membrane crystal has added to the complexity of the resulting TEM projections and until now prevented researchers from recognizing them. It is the added complexity of the oblique sections, though, that allows us to match the TEM projection to a computer simulation of the same with confidence. In this study, formation of cubic membrane structures in amoeba mitochondria was found to be dependent on diet. The cubic structures only occurred in the absence of food, and disappeared in the presence of food, suggesting a structural adaptation and possible advantages for amoeba's survival in nature. The verification of mathematically well-defined structures in unfed amoeba mitochondria is also important to the understanding of the mitochondrial bioenergetics in relation to the topology of the inner membrane, where major cellular energy production as well as free-radical generation are taking place. This understanding may carry great impact upon human health as far as aging and age-related degenerative diseases are concerned, especially as mitochondrial disorders have been implicated in these processes.
Similar content being viewed by others
Abbreviations
- G:
-
gyroid
- D:
-
double diamond
- P:
-
primitive
- TEM:
-
transmission electron microscopy
- PCS:
-
periodic cubic surface
References
Anderson DM, Bellare J, Hoffman JT, Hoffman D, Gunther J, Thomas EL (1992) Algorithms for the computer simulation of two-dimensional projections form structures determined by dividing surfaces. J Colloid Interface Sci 148: 398–414
Andresen N (1956) Cytological investigations on the giant amoeba Chaos chaos L. C R Lab Carlsberg Ser Chim 29: 436–545
Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133: 1251–1263
Bradbury PC (1987) Protozoan adaptations for survival. In: Henis Y (ed) Survival and dormancy of microorganism. Wiley, New York, pp 267–299
Daniels EW, Breyer E (1968) Starvation effects on the ultrastructure of amoeba mitochondria. Z Zellforsch 91: 59–169
Davis ME (1993) Organizing for better synthesis. Nature 364: 391–392
Deng Y (1998) Transmission electron microscopy studies of cubic membrane morphologies in chloroplasts of the green algae Zygnema and mitochondria of the amoeba Chaos carolinensis. PhD dissertation, State University of New York at Buffalo, Buffalo, NY, USA
—, Landh T (1995) The cubic gyroid-based membrane structure of the chloroplast in the Zygnema (Chlorophyceae Zygnematles). Zool Stud 34 Suppl 1: 175–177
Dieuaide M, Couée I, Pradet A, Raymond P (1993) Effect of glucose starvation on the oxidation of fatty acids by maize root tip mitochondria and peroxisomes: evidence for mitochondrial fatty acid β-oxidation and acyl-CoA dehydrogenase activity in a higher plant. Biochem J 296: 199–207
Engström S (1990) Drug delivery from cubic and other lipid-water phases. Lipid Technol 2: 42–45
Ericsson B, Larsson K, Fontell K (1983) A cubic protein-monoolein-water phase. Biochim Biophys Acta 729: 23–27
Holter H, Zeuthen E (1948) Metabolism and reduced weight in starving Chaos chaos. C R Lab Carlsberg Ser Chim 26: 277–296
Journet E, Bligny R, Douce R (1986) Biochemical changes during sucrose deprivation in higher plant cells. J Biol Chem 261: 3193–3199
Kalous M, Drahota Z (1996) The role of mitochondria in aging. Physiol Res 45: 351–359
Lai Y-K, Lee W-C, Hu C-H, Hammond GL (1996) The mitochondria are recognition organelles of cell stress. J Surg Res 62: 90–94
Landau EM, Rosenbusch JP (1996) Lipid cubic phases: a novel concept for the crystallization of membrane proteins. Proc Natl Acad Sci USA 93: 14532–14535
Lambert CA, Radzilowski LL, Thomas EL (1996) Triply periodic level surfaces as models for cubic tricontinuous block copolymer morphologies. Philos Trans R Soc Lond A Math Phys Sci 354: 2009–2023
Landh T (1995) From entangled membranes to eclectic morphologies: cubic membranes as subcellular space organizers. FEBS Lett 369: 13–17
— (1996) Cubic cell membrane architectures: taking another look at membrane bound cell spaces. PhD dissertation, University of Lund, Lund, Sweden
Larsson K (1989) Cubic lipid-water phases: structures and biomembrane aspects. J Phys Chem 93: 7304–7314
—, Fontell K, Krog N (1980) Structural relationships between lamellar, cubic and hexagonal phases in monoglyceride water systems: possibility of cubic structures in biological systems. Chem Phys Lipids 27: 321–328
Lindblom G, Rilfors L (1989) Cubic phases and isotropic structures formed by membrane lipids: possible biological relevance. Biochim Biophys Acta 988: 221–256
Luft R, Landau BR (1995) Mitochondrial medicine. J Int Med 238: 405–421
Luzzati V, Spegt PA (1967) Polymorphism of lipids. Nature 215: 701–704
Mannella CA, Marko M, Penczek P, Barnard D, Frank J (1994) The internal compartmentation of rat-liver mitochondria: tomographic study using high-voltage transmission electron microscope. Microsc Res Tech 27: 278–283
— —, Buttle K (1997) Reconsidering mitochondrial structure: new views of an old organelle. Trends Biochem Sci 22: 37–38
Palade G (1952) The fine structure of mitochondria. Anat Rec 114: 427–451
Pappas GD, Brandt PW (1996) I. Fine structure of complex patterns in the mitochondria of Pleomyxa carolinesis Wilson ( Chaos chaos L.). J Biophys Biochem Cytol 6: 85–90
Pearce P (1978) Structure in nature is a strategy for design. MIT Press, Cambridge, Mass
Perkins G, Renken C, Martone ME, Young SJ, Ellisman M, Fery T (1997) Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. J Struct Biol 119: 260–272
Richeter C, Schweizer M, Cossarizza A, Franceschi C (1996) Control of apoptosis by the cellular ATP level. FEBS Lett 378: 107–110
Schoen AH (1970) Infinite periodic minimal surfaces without self-intersections. NASA Technical Note TN D-5541, National Aeronautics and Space Administration, Washington, DC
Schwarz HA (1890) Gesammelte mathematische Abhandlungen, vol 1. Springer, Berlin
Seddon J (1990) Structure of the inverted hexagonal (HII) phase and non-lamellar phase transitions of lipids. Biochim Biophys Acta 1031: 1–60
Sjöstrand FS (1953) Electron microscopy of mitochondria and cytoplasmic double membranes. Nature 171: 30–31
Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273: 59–63
Thompson GA Jr (1967) Studies of membrane formation in Tetrahymena pryriformis I: rates of phospholipid biosynthesis. Biochemistry 6: 2015–2022
von Schnering HG, Nesper R (1991) Nodal surfaces of Fourier series: fundamental invariants of structured matter. Z Phys B Condensed Matter 83: 407–412
Weindruch R (1996) Caloric restriction and aging. Sci Am 274: 46–52
Wilber CG (1946) The Iipids in Pleomyxa carolinensis. Biol Bull 91: 235
Wojtczak L, Schönfeld P (1993) Effect of fatty acids on energy coupling processes in mitochondria. Biochim Biophys Acta 1183: 41–57
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Deng, Y., Mieczkowski, M. Three-dimensional periodic cubic membrane structure in the mitochondria of amoebae Chaos carolinensis . Protoplasma 203, 16–25 (1998). https://doi.org/10.1007/BF01280583
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01280583