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First published online June 16, 2005
Journal of Experimental Biology 208, 2569-2579 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01660
Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile
1 The Josephine Bay Paul Center for Comparative Molecular Biology and
Evolution, Marine Biological Laboratory, Woods Hole, MA 02543, USA
2 BioCurrents Research Center, Program in Molecular Physiology, Marine
Biological Laboratory, Woods Hole, MA 02543, USA
3 Sea Education Association, PO Box 6, Woods Hole, MA 02543, USA
4 Centro de Biología Molecular, Universidad Autónoma de
Madrid, Cantoblanco, Madrid 28049, Spain
* Author for correspondence (e-mail: mmesserli{at}mbl.edu)
Accepted 25 April 2005
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+
(7x10-8 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+ barriers.
Key words: acidophile, cytosolic pH, membrane potential, energetic cost, Chlamydomonas sp
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