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Review
. 2005 Nov 30;1717(2):67-88.
doi: 10.1016/j.bbamem.2005.09.010. Epub 2005 Sep 26.

Alkaline pH homeostasis in bacteria: new insights

Affiliations
Review

Alkaline pH homeostasis in bacteria: new insights

Etana Padan et al. Biochim Biophys Acta. .

Abstract

The capacity of bacteria to survive and grow at alkaline pH values is of widespread importance in the epidemiology of pathogenic bacteria, in remediation and industrial settings, as well as in marine, plant-associated and extremely alkaline ecological niches. Alkali-tolerance and alkaliphily, in turn, strongly depend upon mechanisms for alkaline pH homeostasis, as shown in pH shift experiments and growth experiments in chemostats at different external pH values. Transcriptome and proteome analyses have recently complemented physiological and genetic studies, revealing numerous adaptations that contribute to alkaline pH homeostasis. These include elevated levels of transporters and enzymes that promote proton capture and retention (e.g., the ATP synthase and monovalent cation/proton antiporters), metabolic changes that lead to increased acid production, and changes in the cell surface layers that contribute to cytoplasmic proton retention. Targeted studies over the past decade have followed up the long-recognized importance of monovalent cations in active pH homeostasis. These studies show the centrality of monovalent cation/proton antiporters in this process while microbial genomics provides information about the constellation of such antiporters in individual strains. A comprehensive phylogenetic analysis of both eukaryotic and prokaryotic genome databases has identified orthologs from bacteria to humans that allow better understanding of the specific functions and physiological roles of the antiporters. Detailed information about the properties of multiple antiporters in individual strains is starting to explain how specific monovalent cation/proton antiporters play dominant roles in alkaline pH homeostasis in cells that have several additional antiporters catalyzing ostensibly similar reactions. New insights into the pH-dependent Na(+)/H(+) antiporter NhaA that plays an important role in Escherichia coli have recently emerged from the determination of the structure of NhaA. This review highlights the approaches, major findings and unresolved problems in alkaline pH homeostasis, focusing on the small number of well-characterized alkali-tolerant and extremely alkaliphilic bacteria.

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Figures

Figure 1
Figure 1
Na+/H+ antiporters, the Na+ cycle and selected H+- and K+-translocating proteins in membranes of four physiologically distinct bacteria. Transporters of the inner membrane of two Gram-negative neutralophilic examples, E. coli and V. cholerae, are schematically depicted within the inner membrane surrounded by the outer membrane. E. coli: a respiratory chain with Q representing ubiquinone or meanquinone, ATP synthase (F0F1) and flagellar motor that are all H+-coupled [236, 237]; both H+- and Na+-coupled solute symporters [238, 239]; and four monovalent cation/proton antiporters, one of which is also a multidrug/proton antiporter [37, 122, 144, 238]. V. cholerae: a respiratory chain that extrudes both Na+ and H+ and H+-coupled ATP synthase; Na+-coupled solute symporters and polar flagellar motor [13, 173] (whereas marine Vibrio species also have H+-coupled lateral flagella [240]); and at least five monovalent cation/proton antiporters; an annotated NhaP and MleN are not shown ([14, 37, 241], www.membranetransport.org). Transporters in Gram-positive neutralophilic B. subtilis and the alkaliphilic species B. pseudofirmus OF4 and Bacillus halodurans C-125 are shown in the cytoplasmic membrane surrounded by a peptidoglycan layer that has associated SCWP (secondary cell wall polymers). The Bacillus species have H+-extruding respiratory chains (MQ=menaquinone), H+-coupled ATP synthases [88, 242, 243], an ABC-type Na+ efflux system [244, 245], and a CPA:2-type K+-extruding system that has been shown to also extrude NH4+ in B. pseudofirmus OF4 [80, 81]. B. subtilis: additionally has both H+- and Na+-coupled solute symporters and flagellar motors [214, 246], five characterized monovalent cation/proton antiporters [–49, 193, 247] and two Ktr-type K+- uptake systems whose ion-coupling properties are not established [136]. B. pseudofirmus OF4 has exclusively Na+-coupled solute symporters and flagellar rotors [88, 214], two monovalent cation/proton antiporters thus far partially characterized [40] and a voltage-gated Na+ channel that plays a role in supporting pH homeostasis as well as chemotaxis and motility[215]. The B. halodurans C-125 genome indicates the presence of MleN and a CPA1 type antiporter [52].
Figure 2
Figure 2
Alkaline pH shift experiments with E. coli and alkaliphilic B. pseudofirmus RAB. A. E. coli cells were grown logarithmically at pH 7.2 in minimal glycerol medium batch cultures before the pH of the medium was adjusted to 8.3 over 30 seconds. A rapid method of cytoplasmic pH and ΔΨ determination in intact cells has made it possible to follow the time course and sequence of changes occuring following the pH shift [58]. Growth was also assed (Klett units). The data are replotted from Figure 3 in reference [58] with permission from the American Society for Microbiology. B. Washed pH 10.5-grown cells of B. pseudofirmus RAB were equilibrated in potassium carbonate buffer at pH 8.5 and then rapidly shifted to pH 10.5 buffer with either 50 mM potassium carbonate (“no Na+”, with or without added AIB), 50 mM sodium carbonate (“Na+”) or 50 mM sodium carbonate + 500 μM AIB. The cytoplasmic pH was monitored after the shift. The figure is a modified version of Figure 3 from reference [61], with permission from the American Society for Biochemistry and Molecular Biology.
Figure 3
Figure 3
Overall architecture of NhaA. A ribbon presentation of the NhaA molecule viewed parallel to the membrane (grey broken line) is shown. The 12 TMSs are labeled with Roman numerals. N and C indicate the N and C termini. Note the unique and novel fold formed by unwinding of helices VI and XI in the middle of the membrane. The remaining short helices at the periplasmic or cytoplasmic sides of the membrane are denoted by p or c respectively. The cytoplasmic and periplasmic funnels are depicted by black line. For further details see [167].
Figure 4
Figure 4
Generation time and PMF parameters of B. pseudofirmus OF4 as a function of external pH in continuous cultures of malate-containing medium. Cells were grown in semi-defined malate containing medium maintained at the indicated pH values. tg, doubling time was calculated from the dilution rates in the chemostat and PMF parameters were determined as described in reference [88]; the data are replotted from Figure 1 of this reference with permission from Blackwell Publishing Ltd.

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