those involved in shuttling of substances across the membrane and electron transport
complexes [150–153]. As aforementioned, there is high presence of proteins in the
membranes of alkaliphiles, and hence, one expects more cardiolipin at elevated pH
to make these protein assortments assemble and function properly. Cardiolipin has a
unique role in membranes involved in OXPHOS, aggregating the proteins involved
in OXPHOS into a patch, and its headgroup serves as H
+ trap [144]. Since
cardiolipin restricts pumped H
+ close to its headgroup domain, it possibly supplies
H
+ to the ATP synthase [144]. Its close association to ATP synthase and respiratory
complexes makes cardiolipin to play a unique role in the bioenergetics of
alkaliphiles. As discussed below in Sect. 3.3.2, alkaliphiles pump out H
+ faster
than non-alkaliphiles, and these protons need to be channeled to ATP synthase
before it dissipates into the bulk phase. To this end, a microcircuit that facilitates
the transfer of H
+ to ATP synthase has been proposed [27]. Based on its close
association to cytochrome c oxidase and ATP synthase, and its unique role in
patching these systems together, trapping H
+ and feeding it to ATP synthase, it
seems that the microcircuit role is, at least partly, played by cardiolipin. Thus, it is
not surprising that alkaliphiles have more cardiolipin in their membrane.
3.3 Bioenergetics
The pH homeostasis which effectively maintains a lower intracellular pH than that of
the extracellular environment comes with bioenergetics challenge, difficulty of
chemiosmotically driven ATP synthesis. Based on the chemiosmotic theory, cells
generate ATP using pmf which is the sum of the transmembrane potential (ΔΨ) and
the H
+ concentration gradient (ΔpH). In non-alkaliphiles, the relatively high concentration of H
+ in extracellular than in intracellular environment results in diffusion
of H
+ to the cell, which is coupled to ATP synthesis by the ATP synthase. However,
in alkaliphiles, this gradient is reversed, the intracellular H
+ concentration exceeds
that of the extracellular, and hence, H
+ cannot diffuse to the cytoplasm. Although
ΔΨ increases at higher pH, it is not high enough to offset the chemiosmotically
counterproductive pH gradient [20, 48, 50, 154]. Thus, it is obvious that the
successful pH homeostasis raises problems concerning H
+ -coupled OXPHOSbased ATP synthesis by prokaryotic alkaliphiles.
In photosynthetic alkaliphiles such as cyanobacteria, the ATP synthase is embedded in thylakoids which are suspended in the cytoplasm and hence not affected by
the extracellular low H
+ concentration [155–157]. The pmf across the thylakoid
membrane is higher than the pmf across the cytoplasmic membrane [158, 159]; thus,
ATP can be produced chemiosmotically regardless of the high pH of their habitat.
Probably, the same holds true for eukaryotic cells (organisms) that are adapted to
high pH habitats and produce ATP using ATP synthase which is partly embedded in
the inner membrane of mitochondria. However, there is no available information on
how eukaryotic organisms thriving in alkaline environments generate ATP through
OXPHOS.
Challenges and Adaptations of Life in Alkaline Habitats
105
complexes [150–153]. As aforementioned, there is high presence of proteins in the
membranes of alkaliphiles, and hence, one expects more cardiolipin at elevated pH
to make these protein assortments assemble and function properly. Cardiolipin has a
unique role in membranes involved in OXPHOS, aggregating the proteins involved
in OXPHOS into a patch, and its headgroup serves as H
+ trap [144]. Since
cardiolipin restricts pumped H
+ close to its headgroup domain, it possibly supplies
H
+ to the ATP synthase [144]. Its close association to ATP synthase and respiratory
complexes makes cardiolipin to play a unique role in the bioenergetics of
alkaliphiles. As discussed below in Sect. 3.3.2, alkaliphiles pump out H
+ faster
than non-alkaliphiles, and these protons need to be channeled to ATP synthase
before it dissipates into the bulk phase. To this end, a microcircuit that facilitates
the transfer of H
+ to ATP synthase has been proposed [27]. Based on its close
association to cytochrome c oxidase and ATP synthase, and its unique role in
patching these systems together, trapping H
+ and feeding it to ATP synthase, it
seems that the microcircuit role is, at least partly, played by cardiolipin. Thus, it is
not surprising that alkaliphiles have more cardiolipin in their membrane.
3.3 Bioenergetics
The pH homeostasis which effectively maintains a lower intracellular pH than that of
the extracellular environment comes with bioenergetics challenge, difficulty of
chemiosmotically driven ATP synthesis. Based on the chemiosmotic theory, cells
generate ATP using pmf which is the sum of the transmembrane potential (ΔΨ) and
the H
+ concentration gradient (ΔpH). In non-alkaliphiles, the relatively high concentration of H
+ in extracellular than in intracellular environment results in diffusion
of H
+ to the cell, which is coupled to ATP synthesis by the ATP synthase. However,
in alkaliphiles, this gradient is reversed, the intracellular H
+ concentration exceeds
that of the extracellular, and hence, H
+ cannot diffuse to the cytoplasm. Although
ΔΨ increases at higher pH, it is not high enough to offset the chemiosmotically
counterproductive pH gradient [20, 48, 50, 154]. Thus, it is obvious that the
successful pH homeostasis raises problems concerning H
+ -coupled OXPHOSbased ATP synthesis by prokaryotic alkaliphiles.
In photosynthetic alkaliphiles such as cyanobacteria, the ATP synthase is embedded in thylakoids which are suspended in the cytoplasm and hence not affected by
the extracellular low H
+ concentration [155–157]. The pmf across the thylakoid
membrane is higher than the pmf across the cytoplasmic membrane [158, 159]; thus,
ATP can be produced chemiosmotically regardless of the high pH of their habitat.
Probably, the same holds true for eukaryotic cells (organisms) that are adapted to
high pH habitats and produce ATP using ATP synthase which is partly embedded in
the inner membrane of mitochondria. However, there is no available information on
how eukaryotic organisms thriving in alkaline environments generate ATP through
OXPHOS.
Challenges and Adaptations of Life in Alkaline Habitats
105