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

Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile
Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile
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+ barriers
0022-0949
2569-2579
Messerli, Mark A.
9181b6bf-b896-43ae-a7c0-f8c12bf17d46
Amaral-Zettler, Linda A.
e6692f99-ea32-4a4e-a194-5f88c31b109f
Zettler, Erik
b1c853be-fc2f-4550-8d47-85f7d38667f4
Jung, Sung-Kwon
9b10457b-933f-4247-a75a-62320f744dc7
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Sogin, Mitchell L.
23f8a287-ebed-4706-800a-9fe8022b9f55
Messerli, Mark A.
9181b6bf-b896-43ae-a7c0-f8c12bf17d46
Amaral-Zettler, Linda A.
e6692f99-ea32-4a4e-a194-5f88c31b109f
Zettler, Erik
b1c853be-fc2f-4550-8d47-85f7d38667f4
Jung, Sung-Kwon
9b10457b-933f-4247-a75a-62320f744dc7
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Sogin, Mitchell L.
23f8a287-ebed-4706-800a-9fe8022b9f55

Messerli, Mark A., Amaral-Zettler, Linda A., Zettler, Erik, Jung, Sung-Kwon, Smith, Peter J.S. and Sogin, Mitchell L. (2005) Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile. Journal of Experimental Biology, 208 (13), 2569-2579. (doi:10.1242/?jeb.01660). (PMID:15961743)

Record type: Article

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+ barriers

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Published date: July 2005
Organisations: University of Southampton

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Local EPrints ID: 188819
URI: http://eprints.soton.ac.uk/id/eprint/188819
ISSN: 0022-0949
PURE UUID: 5032b299-842e-43df-9ce1-e599cc4204d3
ORCID for Peter J.S. Smith: ORCID iD orcid.org/0000-0003-4400-6853

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Date deposited: 06 Jun 2011 08:17
Last modified: 03 Dec 2019 01:40

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Contributors

Author: Mark A. Messerli
Author: Linda A. Amaral-Zettler
Author: Erik Zettler
Author: Sung-Kwon Jung
Author: Mitchell L. Sogin

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