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Potassium stress growth characteristics and energetics in the haloarchaeon Haloarcula marismortui.

Jensen MW, Matlock SA, Reinheimer CH, Lawlor CJ, Reinheimer TA, Gorrell A - Extremophiles (2014)

Bottom Line: The presence of intracellular rubidium and cesium indicates that monovalent ion transport is important for energy production.Comparison of eight archaeal genomes indicates an increased diversity of potassium transport complex subunits in the halophilic organisms.Analysis of the generation times, intracellular concentrations and genome survey shows Har. marismortui exhibits an ability to cope with monovalent cation concentration changes in its native environment and provides insight into the organisms ion transport capability and specificity.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, University of Northern British Columbia, 3333 University Way, Prince George, BC, V2N 4Z9, Canada.

ABSTRACT
Growth characteristics surrounding halophilic archaeal organisms are extremely limited in the scientific literature, with studies tending toward observing changes in cellular generation times under growth conditions limited to changes in temperature and sodium chloride concentrations. Currently, knowledge of the ionic stress experienced by haloarchaeal species through an excess or depletion of other required ions is lacking at best. The halophilic archaeon, Haloarcula marismortui, was analyzed under extreme ionic stress conditions with a specific focus on induced potassium ion stress using growth curves and analysis of the intracellular ion concentrations. Generation times were determined under potassium chloride concentrations ranging from 8 to 720 mM, and also in the presence of the alternative monovalent cations of lithium, rubidium, and cesium under limiting potassium conditions. Intracellular ion concentrations, as determined by inductively coupled mass spectrometry (ICP-MS), indicate a minimum intracellular total ion requirement of 1.13 M while tolerating up to 2.43 M intracellular concentrations. The presence of intracellular rubidium and cesium indicates that monovalent ion transport is important for energy production. Comparison of eight archaeal genomes indicates an increased diversity of potassium transport complex subunits in the halophilic organisms. Analysis of the generation times, intracellular concentrations and genome survey shows Har. marismortui exhibits an ability to cope with monovalent cation concentration changes in its native environment and provides insight into the organisms ion transport capability and specificity.

Show MeSH
Ion transport systems in Har. marismortui. Ion flow in the haloarchaeon, Har. marismortui as modeled after Oren et al. (1990) illustrating ion flow within cells. Proton flow in and out of the cell and relative ion concentrations are emphasized to show formation of the proton motive force and ion gradients. Classes are as described in Table 3. The new subclass 6A is defined for K+/H+ symport, which uses the proton motive force to drive K+ sequestration through the Trk system. Sodium transport for class 8 transporters is included as co-transport with chloride (Duschl and Wagner 1986)
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Fig4: Ion transport systems in Har. marismortui. Ion flow in the haloarchaeon, Har. marismortui as modeled after Oren et al. (1990) illustrating ion flow within cells. Proton flow in and out of the cell and relative ion concentrations are emphasized to show formation of the proton motive force and ion gradients. Classes are as described in Table 3. The new subclass 6A is defined for K+/H+ symport, which uses the proton motive force to drive K+ sequestration through the Trk system. Sodium transport for class 8 transporters is included as co-transport with chloride (Duschl and Wagner 1986)

Mentions: The Trk system does not hydrolyze ATP to function, but rather utilizes it for regulatory purposes only (Stewart et al.), and as noted by Oren (1999) it is possible that an increased demand for potassium uptake through the Trk system could immobilize a substantial quantity of ATP. If regulation occurs through the binding of ATP in a transporter active site or allosteric site, the ATP available for other cellular processes would become limited. Additionally, the recognition of Trk as a K+/H+ symporter (Stewart et al. 1985) allows potassium sequestering to be driven by the proton motive force in Har. marismortui, without the requirement for a high-affinity ATPase. This agrees with the finding that no ATP-driven potassium transport was identified in the genome survey and provides a second possible explanation for the observed changes in generation time. Considering the known ion transport systems (Fig. 4), a decrease in total cellular energy availability due to ATP sequestration for the regulation of the Trk symport system would result in a depletion of the cellular ATP pool. This has lead to the sub-division of Oren’s (1999) potassium transport class (class 6; Fig. 4) to a potassium transport and a K+/H+ symport class (class 6 and 6A, respectively; Fig. 4). It would be worthwhile to investigate changes in the Har. marismortui ATP pool through each stage of growth to provide further evidence for this proposed mode of potassium transport and to confirm that these changes in ATP concentration actually occur in response to changes in extracellular potassium concentrations.Fig. 4


Potassium stress growth characteristics and energetics in the haloarchaeon Haloarcula marismortui.

Jensen MW, Matlock SA, Reinheimer CH, Lawlor CJ, Reinheimer TA, Gorrell A - Extremophiles (2014)

Ion transport systems in Har. marismortui. Ion flow in the haloarchaeon, Har. marismortui as modeled after Oren et al. (1990) illustrating ion flow within cells. Proton flow in and out of the cell and relative ion concentrations are emphasized to show formation of the proton motive force and ion gradients. Classes are as described in Table 3. The new subclass 6A is defined for K+/H+ symport, which uses the proton motive force to drive K+ sequestration through the Trk system. Sodium transport for class 8 transporters is included as co-transport with chloride (Duschl and Wagner 1986)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4339784&req=5

Fig4: Ion transport systems in Har. marismortui. Ion flow in the haloarchaeon, Har. marismortui as modeled after Oren et al. (1990) illustrating ion flow within cells. Proton flow in and out of the cell and relative ion concentrations are emphasized to show formation of the proton motive force and ion gradients. Classes are as described in Table 3. The new subclass 6A is defined for K+/H+ symport, which uses the proton motive force to drive K+ sequestration through the Trk system. Sodium transport for class 8 transporters is included as co-transport with chloride (Duschl and Wagner 1986)
Mentions: The Trk system does not hydrolyze ATP to function, but rather utilizes it for regulatory purposes only (Stewart et al.), and as noted by Oren (1999) it is possible that an increased demand for potassium uptake through the Trk system could immobilize a substantial quantity of ATP. If regulation occurs through the binding of ATP in a transporter active site or allosteric site, the ATP available for other cellular processes would become limited. Additionally, the recognition of Trk as a K+/H+ symporter (Stewart et al. 1985) allows potassium sequestering to be driven by the proton motive force in Har. marismortui, without the requirement for a high-affinity ATPase. This agrees with the finding that no ATP-driven potassium transport was identified in the genome survey and provides a second possible explanation for the observed changes in generation time. Considering the known ion transport systems (Fig. 4), a decrease in total cellular energy availability due to ATP sequestration for the regulation of the Trk symport system would result in a depletion of the cellular ATP pool. This has lead to the sub-division of Oren’s (1999) potassium transport class (class 6; Fig. 4) to a potassium transport and a K+/H+ symport class (class 6 and 6A, respectively; Fig. 4). It would be worthwhile to investigate changes in the Har. marismortui ATP pool through each stage of growth to provide further evidence for this proposed mode of potassium transport and to confirm that these changes in ATP concentration actually occur in response to changes in extracellular potassium concentrations.Fig. 4

Bottom Line: The presence of intracellular rubidium and cesium indicates that monovalent ion transport is important for energy production.Comparison of eight archaeal genomes indicates an increased diversity of potassium transport complex subunits in the halophilic organisms.Analysis of the generation times, intracellular concentrations and genome survey shows Har. marismortui exhibits an ability to cope with monovalent cation concentration changes in its native environment and provides insight into the organisms ion transport capability and specificity.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, University of Northern British Columbia, 3333 University Way, Prince George, BC, V2N 4Z9, Canada.

ABSTRACT
Growth characteristics surrounding halophilic archaeal organisms are extremely limited in the scientific literature, with studies tending toward observing changes in cellular generation times under growth conditions limited to changes in temperature and sodium chloride concentrations. Currently, knowledge of the ionic stress experienced by haloarchaeal species through an excess or depletion of other required ions is lacking at best. The halophilic archaeon, Haloarcula marismortui, was analyzed under extreme ionic stress conditions with a specific focus on induced potassium ion stress using growth curves and analysis of the intracellular ion concentrations. Generation times were determined under potassium chloride concentrations ranging from 8 to 720 mM, and also in the presence of the alternative monovalent cations of lithium, rubidium, and cesium under limiting potassium conditions. Intracellular ion concentrations, as determined by inductively coupled mass spectrometry (ICP-MS), indicate a minimum intracellular total ion requirement of 1.13 M while tolerating up to 2.43 M intracellular concentrations. The presence of intracellular rubidium and cesium indicates that monovalent ion transport is important for energy production. Comparison of eight archaeal genomes indicates an increased diversity of potassium transport complex subunits in the halophilic organisms. Analysis of the generation times, intracellular concentrations and genome survey shows Har. marismortui exhibits an ability to cope with monovalent cation concentration changes in its native environment and provides insight into the organisms ion transport capability and specificity.

Show MeSH