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Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile

By Mark A. Messerli, Linda A. Amaral-Zettler, Erik Zettler, Sung-Kwon Jung, Peter J.S. Smith and Mitchell L. Sogin

Abstract

Organisms growing in acidic environments, pH <3, would be expected to possess fundamentally different molecular structures and physiological controls in comparison with similar species restricted to neutral pH. We begin to investigate this premise by determining the magnitude of the transmembrane electrochemical H+ gradient in an acidophilic Chlamydomonas sp. (ATCC® PRA-125) isolated from the Rio Tinto, a heavy metal laden, acidic river (pH 1.7-2.5). This acidophile grows most rapidly at pH 2 but is capable of growth over a wide pH range (1.5-7.0), while Chlamydomonas reinhardtii is restricted to growth at pH ?3 with optimal growth between pH 5.5 and 8.5. With the fluorescent H+ indicator, 2?,7?-bis-(2-carboxyethyl)-5-(and-6)-carboxyfluorescein (BCECF), we show that the acidophilic Chlamydomonas maintains an average cytosolic pH of 6.6 in culture medium at both pH 2 and pH 7 while Chlamydomonas reinhardtii maintains an average cytosolic pH of 7.1 in pH 7 culture medium. The transmembrane electric potential difference of Chlamydomonas sp., measured using intracellular electrodes at both pH 2 and 7, is close to 0 mV, a rare value for plants, animals and protists. The 40 000-fold difference in [H+] could be the result of either active or passive mechanisms. Evidence for active maintenance was detected by monitoring the rate of ATP consumption. At the peak, cells consume about 7% more ATP per second in medium at pH 2 than at pH 7. This increased rate of consumption is sufficient to account for removal of H+ entering the cytosol across a membrane with relatively high permeability to H+ (7×10-8 cm s-1). Our results indicate that the small increase in the rate of ATP consumption can account for maintenance of the transmembrane H+ gradient without the imposition of cell surface H+ barrier

Topics: QH301
Year: 2005
OAI identifier: oai:eprints.soton.ac.uk:188819
Provided by: e-Prints Soton

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  1. (1999). A comparative ecological study of two acidic rivers in southwestern Spain. doi
  2. (2001). A new iron oxidase from a moderately thermophilic iron oxidizing bacterium strain TI-1. doi
  3. (1998). Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Picrophilus oshimae. doi
  4. (1987). Cell-wall lytic enzymes (autolysins) of Chlamydomonas reinhardtii are (hydroxy)proline-specific proteases. doi
  5. (1991). Characterization of a plasma membrane H+-ATPase from the extremely acidophilic alga Dunaliella acidophila. doi
  6. (1999). Direct measurement of cytosolic calcium and pH in living Chlamydomonas reinhardtii cells. doi
  7. (1989). Dunaliella acidophila (Kalina) Masyuk – an alga with a positive membrane potential. doi
  8. (1995). Effects of cobalt and pH on the growth of Chlamydomonas reinhardtii. doi
  9. (1981). Effects of environmental pH on the internal pH of Chlorella pyrenoidosa, Scenedesmus quadricauda, and Euglena mutabilis. doi
  10. (1988). Effects of NaCl, Na2SO4, H2SO4 and glucose on growth, photosynthesis, and respiration in the acidophilic alga Dunaliella acidophila (Volvocales, doi
  11. (1999). Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. doi
  12. (2002). Eukaryotic diversity in Spain’s River of Fire. doi
  13. (1984). Internal pH of the obligate acidophile Cyanidium caldarium Geitler (Rhodophyta?). doi
  14. (1976). Intracellular pH measurements with a spectroscopic probe generated in situ.
  15. (1986). Intracellular pH regulation in an acidophilic unicellular alga, Cyanidium caldarium: 31P-NMR determination of intracellular pH.
  16. (1983). KCl leakage from microelectrodes and its impact on the membrane parameters of a nonexcitable cell. doi
  17. (1998). Low permeability of liposomal membranes composed of bipolar tetraether lipids from thermoacidophilic archaebacterium Sulfolobus acidocaldarius. doi
  18. (1992). Measurement of the transmembrane electrical potential of Dunaliella acidophila by microelectrodes. doi
  19. (1975). Mechanisms of the acidoand thermo-phily of Cyanidium caldarium Geitler II. Physiological role of the cell wall.
  20. (1997). Messerli and others THE JOURNAL OF EXPERIMENTAL BIOLOGY2579 Increased energetic cost for eukaryotic acidophile doi
  21. (2001). Microbial community composition and ecology of an acidic aquatic environment: The Tinto River,
  22. (1996). On the mechanism of hyperacidification in lemon, comparison of the vacuolar H+-ATPase of fruits and epicotyls. doi
  23. (2002). Osmoregulation and contractile vacuoles of protozoa. doi
  24. (1999). Oxygen microsensor and its application to single cells and mouse pancreatic islets. doi
  25. (1987). Physiological adaptations of anaerobic bacteria to low pH: metabolic control of proton motive force in Sarcina ventriculi.
  26. (1996). Primary structure and effect of pH on the expression of the plasma membrane H+-ATPase from Dunaliella acidophila and Dunaliella salina. doi
  27. (1984). Proton/hydroxide conductance through lipid bilayer membranes. doi
  28. (1995). Purification and characterization of a vegetative lytic enzyme responsible for liberation of daughter cells during the proliferation of Chlamydomonas reinhardtii.
  29. (2001). Purification and properties of thiosulfate dehydrogenase from Acidithiobacillus thiooxidans JCM7814. doi
  30. (1998). Reconstructing past ocean pH-depth profiles. doi
  31. (1981). Role of the plasma membrane proton pump in pH regulation in non-animal cells. doi
  32. (1994). Role of water in proton conductance across model and biological membranes. doi
  33. (1999). Specific metal sequestering acidophilic fungi. doi
  34. (2002). The ionic composition of the contractile vacuole fluid of Paramecium mirrors ion transport across the plasma membrane. doi
  35. (1971). The physiological ecology of Cyanidium caldarium. doi
  36. (1994). Two distinct, calcium-mediated, signal transduction pathways can trigger deflagellation in Chlamydomonas reinhardtii. doi
  37. (1994). Unique permeability barrier of the apical surface of parietal and chief cells in isolated perfused gastric glands.

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