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

Abstract

Extremely acidic aquatic environments, <pH·3, are rare in comparison to the neutral and slightly alkaline conditions that occur in open lakes and oceans (Wetzel, 1975;Palmer et al., 1998). The Rio Tinto, in Southwestern Spain, is one such extreme environment. The river extends 90·km, with a pH range of 1.7-2.5 over its entire length. (López-Archilla and Amils, 1999). Despite these seemingly toxic conditions, protists, fungi and bacteria (Amaral Zettler et al., 2002;Durán et al., 1999;López-Archilla et al., 2001), thrive in the river. In nature, acidic conditions, such as in the stomach of higher organisms or within any of the many forms of acidic lysosomes, are used to denature and destroy macromolecules and to control specially made hydrolytic enzymes that speed the rate of molecular breakdown. It is, therefore, of fundamental biochemical and physiological interest to understand how these organisms are modified to be acid tolerant.In order to identify the adaptations used to survive in acid, we need to consider first which components of acidophiles are in contact with low pH. For example, acidophilic bacteria have cell surface enzymes that have acid pH optima. A surface iron oxidase from bacterial strain TI-1 has a pH optimum of 3.0 (Takai et al., 2001) while a surface thiosulfate dehydrogenase from Acidithiobacillus thiooxidans has a pH optimum of 3.5 (Nakamura et al., 2001). Protistan extremophiles must also cope with acid conditions on the surface of the plasma membrane. Ion channels and transporters are in contact with

Knockdown of limiting-CO 2 –induced gene HLA3 decreases HCO 3 − transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii

“…21), and the pH-dependence of the HLA3 knockdown phenotypes argues strongly for a plasma membrane localization. The cytosolic pH of C. reinhardtii is relatively stable to external pH changes over its optimal growth range of pH 5.5-8.5 (26,27), so the observed high-pH-dependent decrease in Ci affinity of HLA3 knockdown strains indirectly argues for the plasma membrane as the probable location of HLA3.…”

Early eukaryotic origins for cilia-associated bioactive peptide-amidating activity

“…The topology of the protein in the cilium places the enzymatic domains in the extracellular milieu. Chlamydomonas reinhardtii grows above pH 3 and exhibits maximal growth rates in the range pH 5.5-8.5, conditions where both PHM and PAL can be active (Messerli et al, 2005). Extracellular environments containing oxygen and single electron donors might well support PAM enzyme activity.…”

Environmental controls on coccolithophore calcification

“…The additional energy requirement for intracellular pH regulation is probably not more than 1% or so of respiratory energy output; intracellular pH regulation in an acidophilic Chlamydomonas species growing at an external pH of 2 uses less than 7% of the respiratory energy output (Messerli et al 2005, Raven 2011a). …”