Effect of Temperature on Glycerol Retention in the Halotolerant Algae <i>Dunaliella</i> and <i>Asteromonas</i>

Wegmann, K.; Ben‐Amotz, Ami; Avron, Mordhay

doi:10.1104/pp.66.6.1196

Cited by 62 publications

(28 citation statements)

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“…The glpA1B1C1, glpK, glpF (encoding a putative glycerol facilitator), and ptsH2 (encoding a homolog of the bacterial phosphotransferase system protein Hpr) genes were transcriptionally linked and appeared to be under the control of a strong, G3P-inducible promoter upstream of glpA1. Overall, this study provides fundamental insights into glycerol metabolism in H. volcanii and enhances our understanding of central metabolic pathways of haloarchaea.Glycerol is a highly abundant energy source in hypersaline environments as a result of leakage from and lysis of Dunaliella cells, which are known to accumulate glycerol in molar quantities as an organic, osmotic solute (3,5,7,32). Thus, glycerol is a primary energy source for heterotrophic members of this community.…”

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Activity and Transcriptional Regulation of Bacterial Protein-Like Glycerol-3-Phosphate Dehydrogenase of the Haloarchaea in Haloferax volcanii

2011

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Glycerol is a primary energy source for heterotrophic haloarchaea and a major component of "salty" biodiesel waste. Glycerol is catabolized solely by glycerol kinase (encoded by glpK) to glycerol-3-phosphate (G3P) in Haloferax volcanii. Here we characterized the next critical step of this metabolic pathway: the conversion of G3P to dihydroxyacetone phosphate by G3P dehydrogenase (G3PDH). H. volcanii harbors two putative G3PDH operons: (i) glpA1B1C1, located on the chromosome within the neighborhood of glpK, and (ii) glpA2B2C2, on megaplasmid pHV4. Analysis of knockout strains revealed that glpA1 (and not glpA2) is required for growth on glycerol. However, both glpA1 and glpA2 could complement a glpA1 knockout strain (when expressed from a strong promoter in trans) and were required for the total G3PDH activity of cell lysates. The glpA1B1C1, glpK, glpF (encoding a putative glycerol facilitator), and ptsH2 (encoding a homolog of the bacterial phosphotransferase system protein Hpr) genes were transcriptionally linked and appeared to be under the control of a strong, G3P-inducible promoter upstream of glpA1. Overall, this study provides fundamental insights into glycerol metabolism in H. volcanii and enhances our understanding of central metabolic pathways of haloarchaea.Glycerol is a highly abundant energy source in hypersaline environments as a result of leakage from and lysis of Dunaliella cells, which are known to accumulate glycerol in molar quantities as an organic, osmotic solute (3,5,7,32). Thus, glycerol is a primary energy source for heterotrophic members of this community.In biological systems, glycerol is metabolized to dihydroxyacetone phosphate (DHAP) by one of two routes: (i) phosphorylation by glycerol kinase and subsequent conversion of sn-glycerol-3-phosphate (G3P) into DHAP through G3P dehydrogenase (G3PDH) or (ii) oxidation by glycerol dehydrogenase to form dihydroxyacetone (DHA), which is subsequently phosphorylated by an ATP-dependent or phosphoenolpyruvate:phosphotransferase system (PEP:PTS)-dependent DHA kinase to form DHAP. Once generated from glycerol, DHAP can be channeled into metabolic intermediates, including pyruvate, G3P, and/or sn-glycerol-1-phosphate (G1P).Recently, we demonstrated through Haloferax volcanii that haloarchaea require glycerol kinase (encoded by glpK) for the catabolism of glycerol (27). These results suggest that (i) G3PDH is needed for glycerol metabolism and (ii) the homologs of bacterial PEP:PTS-dependent DHA kinase are not needed for glycerol catabolism in H. volcanii but may serve in the metabolism of DHA overflow products generated by other members of the hypersaline community, such as Dunaliella salina (4).In this study, we investigated the oxidation of G3P to DHAP by G3PDH, a metabolic step likely to be central to glycerol catabolism and subsequent to the phosphorylation of glycerol by glycerol kinase in haloarchaea. Since archaea use G1PDH (encoded by egsA) to convert DHAP to G1P for the biosynthesis of phospholipids, G3PDH homologs are not common in this d...

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“…Glycerol is a highly abundant energy source in hypersaline environments as a result of leakage from and lysis of Dunaliella cells, which are known to accumulate glycerol in molar quantities as an organic, osmotic solute (3,5,7,32). Thus, glycerol is a primary energy source for heterotrophic members of this community.…”

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Activity and Transcriptional Regulation of Bacterial Protein-Like Glycerol-3-Phosphate Dehydrogenase of the Haloarchaea in Haloferax volcanii

2011

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“…Glycerol levels seem to be only dictated by the rate of glycerol synthesis that must be accelerated during the accumulation period and deactivated during the decrease period. The direct dephosphorylation of the G3P to glycerol has been proposed to be the pathway used in smelt to directly produce glycerol (5,8), as it is the case in some algae and yeasts producing high amounts of glycerol in response to environmental stresses (23,37). Activity of such an enzyme has been suggested in oxygenlimited rat heart and brain, although neither the protein nor the transcript have been identified in a vertebrate (4,22).…”

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Glycerol loss to water exceeds glycerol catabolism via glycerol kinase in freeze-resistant rainbow smelt (Osmerus mordax)

Ditlecadet

Short

Driedzic

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Rainbow smelt accumulate high amounts of glycerol in winter. In smelt, there is a predictable profile of plasma glycerol levels that starts to increase in November (<5 μmol/ml), peaks in mid-February (>200 μmol/ml), and thereafter decreases to reach the initial levels in the beginning of May. The aim of this study was to investigate the respective role of the two main mechanisms that might be involved in glycerol clearance from mid-February: 1) breakdown of glycerol to glycerol-3-phosphate through the action of the glycerol kinase (GK) and 2) direct loss toward the environment. Over the entire glycerol cycle, loss to water represents a daily loss of ∼10% of the total glycerol content of fish. GK activities were very low in all tissues investigated and likely have a minor quantitative role in the glycerol cycle. These results suggest that glycerol levels are dictated by the rate of glycerol synthesis (accelerated and deactivated during the accumulation and decrease stages, respectively). Although not important in glycerol clearance, GK in liver might have an important metabolic function for other purposes, such as gluconeogenesis, as evidenced by the significant increase of activity at the end of the cycle.

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“…Assay of Glycerol. Three ml of A. gracilis suspension in the culture medium were transferred to a test tube and placed in a water bath maintained at about 70 C for 10 min (18). The samples were centrifuged at room temperature for 5 min at 2000g and the glycerol content of the supernatant was determined chemically as previously described (4).…”

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Osmoregulation in the Halotolerant Alga Asteromonas gracilis

Ben‐Amotz¹,

Grunwald²

1981

Plant Physiol.

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Asteromonas gracilis, a green wall-less halotolerant alga, grows on salt concentrations from 0.5 molar NaCl (seawater) to saturation (4.5 molar NaCI). The specific growth rate was maximal at concentrations between 0.5 and 2.5 molar and only graduaDly decreased above 2.5 molar. Photosynthetic oxygen evolution was maximal over a range of salinities around 2.5 molar and the photosynthesis to respiration ratio showed a maximum at 1.5 molar NaCI. The alga accumulates large amounts of intraceDlular glycerol in response to saline conditions. The glycerol content of the cells varied in direct proportion to the extracellular salt concentration, being about 50 and 400 picograms glycerol per cell in algae grown at 0.5 and 4.5 molar NaCI, respectively. In salt concentrations lower than 3.5 molar and at growth temperatures below 40 C, essentialy al the glycerol was intraceHular. Above 3.5 molar NaCI, about 25 per cent of the total glycerol leaked slowly from the cels to the medium. Treating the algae for several minutes at temperatures exceeding 47 C caused 50 per cent release of the internal glycerol. At 60 C, 100 per cent of the glycerol was released. When the extraceHular salt concentration was increased or decreased, the intracelular glycerol varied accordingly, reaching its new intracelular level after a few hours. Both photosynthesis and respiration were inhibited on transfer of the cels from 1.5 to 3.5 molar NaCI but were not inhibited on transfer of the cels from 3.5 to 1.5 molar NaCI. The kinetics of photosynthetic resumption preceded the kinetics of glycerol biosynthesis. The above results indicate the existence of osmotic regulations in Asteromonasgracilis via the accumulation of intracelular glycerol.Asteromonas gracilis Artari is a green wall-less unicellular flagellate of the class Prasinophyceae present in salt marshes and small brine ponds (10,15,17,19,20). The algae are often subjected to widely fluctuating salt concentrations and can tolerate a broad range of salt, from low salinity to saturated NaCl solutions. In contrast to the many studies which were undertaken on the halotolerant alga Dunaliella (9) to elucidate the mechanism of its osmotic adaptation under salt stress (2, 4-8), the information on osmoregulation in Asteromonas is rather limited. Recently BenAmotz and Avron (5) showed that Asteromonas and Dunaliella produce and accumulate glycerol to a concentration isoosmotic with the medium and, thus, are able to survive in saline water. The communication presented here describes an investigation of the physiological behavior of A. gracilis under salt stress.

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Effect of Temperature on Glycerol Retention in the Halotolerant Algae Dunaliella and Asteromonas

Cited by 62 publications

References 6 publications

Activity and Transcriptional Regulation of Bacterial Protein-Like Glycerol-3-Phosphate Dehydrogenase of the Haloarchaea in Haloferax volcanii

Activity and Transcriptional Regulation of Bacterial Protein-Like Glycerol-3-Phosphate Dehydrogenase of the Haloarchaea in Haloferax volcanii

Glycerol loss to water exceeds glycerol catabolism via glycerol kinase in freeze-resistant rainbow smelt (Osmerus mordax)

Osmoregulation in the Halotolerant Alga Asteromonas gracilis

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