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Chapter 7 : The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles

Authors: Helena Santos1, Pedro Lamosa2, Tiago Q. Faria3, Nuno Borges4, ClÉlia Neves5
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Affiliations: 1: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, Apartado 127, 2780-156 Oeiras, Portugal; 2: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, Apartado 127, 2780-156 Oeiras, Portugal; 3: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, Apartado 127, 2780-156 Oeiras, Portugal; 4: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, Apartado 127, 2780-156 Oeiras, Portugal; 5: Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Rua da Quinta Grande 6, Apartado 127, 2780-156 Oeiras, Portugal
Content Type: Monograph
Publication Year: 2007

Category: Applied and Industrial Microbiology; Environmental Microbiology

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Abstract:

Many thermophiles and hyperthermophiles (from now on designated (hyper)thermophiles) have been isolated from both fresh water and seawater sources. Compatible solutes must be highly soluble and they usually belong to one of the following groups of compounds: amino acids, sugars, polyols, betaines, and ectoines. In general, compatible solutes accumulate to high levels in the cytoplasm. The relative abundance combined with the low molecular mass of these compounds greatly facilitates the task of their molecular identification by resorting to two powerful analytical techniques: nuclear magnetic resonance (NMR) and mass spectrometry. The mannosyl-3-phosphoglycerate synthase (MPGS) characterized to date produce mannosyl-3-phosphoglycerate with the same anomeric configuration of the substrate and accordingly have been classified as members of glycosyltransferases family GT55, which comprises GDP-mannose: α-mannosyltransferases that retain the anomeric configuration of the substrate. The evolution of MG biosynthesis is a fascinating topic but a meaningful discussion would demand more ample data sets and reliable tools for genome analysis. Diglycerol phosphate (DGP) biosynthesis was investigated by the author and his team on . In the case of solutes from hyperthermophiles, it was shown that the protecting effect was clearly dependent on the solute charge. The melting temperature of bovine ribonuclease A (RNase A) in the presence and absence of 2-a-O-mannosylglycerate (MG) depends on the ionization state of the solute. Due to the enhanced ability to stabilize biological materials, the application of hypersolutes in industrial applications was soon envisioned, and several industrial patents on their uses have been filed.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles
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Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
/content/10.1128/9781555815813.ch07.ch07fig01
Figure 1.
Compatible solutes primarily restricted to hyperthermophiles.
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Image of Figure 1.
Figure 1.

Compatible solutes primarily restricted to hyperthermophiles.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 2.
Distribution of trehalose (circles), mannosylglycerate (diamonds) and di--inositol-1,1′-phosphate (stars) among (hyper)thermophiles. Tree of Life adapted from . The question marks indicate unknown positions of the branching points between the three domains.
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Image of Figure 2.
Figure 2.

Distribution of trehalose (circles), mannosylglycerate (diamonds) and di--inositol-1,1′-phosphate (stars) among (hyper)thermophiles. Tree of Life adapted from . The question marks indicate unknown positions of the branching points between the three domains.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 3.
The two pathways for the synthesis of mannosylglycerate in . Single-step pathway uses mannosylglycerate synthase (MGS), while the two-step pathway involves the actions of mannosyl-3-phosphoglycerate synthase (MPGS) and mannosyl-3-phosphoglycerate phosphatase (MPGP).
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Image of Figure 3.
Figure 3.

The two pathways for the synthesis of mannosylglycerate in . Single-step pathway uses mannosylglycerate synthase (MGS), while the two-step pathway involves the actions of mannosyl-3-phosphoglycerate synthase (MPGS) and mannosyl-3-phosphoglycerate phosphatase (MPGP).

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 4.
Unrooted phylogenetic tree based on known or putative sequences of mannosyl-3-phosphoglycerate synthase genes. The ClustalX and TreeView programs 5,7 were used for sequence alignment and to generate the phylogenetic tree. The significance of the branching order was evaluated by bootstrap analysis of 1000 computer-generated trees. Bar, 0.1 change per site. Abbreviations: Aper, ; Apro, ; Aven, ; Deth, ; Mgri, ; Ncra, ; Pfer, ; Paby, ; Pfur, ; Phor, ; Rmar, ; Tthe, ; Tlit, .
10.1128/9781555815813/f0094-01_thmb.gif
10.1128/9781555815813/f0094-01.gif
Image of Figure 4.
Figure 4.

Unrooted phylogenetic tree based on known or putative sequences of mannosyl-3-phosphoglycerate synthase genes. The ClustalX and TreeView programs 5,7 were used for sequence alignment and to generate the phylogenetic tree. The significance of the branching order was evaluated by bootstrap analysis of 1000 computer-generated trees. Bar, 0.1 change per site. Abbreviations: Aper, ; Apro, ; Aven, ; Deth, ; Mgri, ; Ncra, ; Pfer, ; Paby, ; Pfur, ; Phor, ; Rmar, ; Tthe, ; Tlit, .

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 5.
Genomic organization of mannosylglycerate biosynthesis via the two-step pathway. Black arrows indicate genes; dark grey arrows indicate the genes; light grey arrow represents the phosphomannose isomerase/mannose-1-phosphate guanylyltransferase; the white arrow indicates phosphomannomutase.
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Image of Figure 5.
Figure 5.

Genomic organization of mannosylglycerate biosynthesis via the two-step pathway. Black arrows indicate genes; dark grey arrows indicate the genes; light grey arrow represents the phosphomannose isomerase/mannose-1-phosphate guanylyltransferase; the white arrow indicates phosphomannomutase.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 6.
Dependence of the melting temperature of RNase A on pH in the absence of solutes (squares and thin line) and with 0.5 M mannosylglycerate (circles and thick line).
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Image of Figure 6.
Figure 6.

Dependence of the melting temperature of RNase A on pH in the absence of solutes (squares and thin line) and with 0.5 M mannosylglycerate (circles and thick line).

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 7.
Effect of solutes on the melting temperature of staphylococcal nuclease (SNase) and pig heart malate dehydrogenase (MDH). Abbreviations: Tre, trehalose; MG, α-mannosylglycerate; MGA, α-mannosylglyceramide; DIP, di- -inositol-1,1′-phosphate; DGP, diglycerol phosphate; KCl, potassium chloride; Gly, glycerol; Ect, ectoine; Hect, hydroxyectoine.
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10.1128/9781555815813/f0098-01.gif
Image of Figure 7.
Figure 7.

Effect of solutes on the melting temperature of staphylococcal nuclease (SNase) and pig heart malate dehydrogenase (MDH). Abbreviations: Tre, trehalose; MG, α-mannosylglycerate; MGA, α-mannosylglyceramide; DIP, di- -inositol-1,1′-phosphate; DGP, diglycerol phosphate; KCl, potassium chloride; Gly, glycerol; Ect, ectoine; Hect, hydroxyectoine.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 8.
Schematic representation of the preferential exclusion of solutes from the protein surface in the native and unfolded states. Upon denaturation, the zone of exclusion increases and, although the same amount of solute molecules is depicted, these become locally more concentrated, i.e., their chemical potential has increased. As a consequence, to achieve thermodynamic equilibrium, the unfolding reaction is displaced to the native state, hence the solute acts as a stabilizer.
10.1128/9781555815813/f0099-01_thmb.gif
10.1128/9781555815813/f0099-01.gif
Image of Figure 8.
Figure 8.

Schematic representation of the preferential exclusion of solutes from the protein surface in the native and unfolded states. Upon denaturation, the zone of exclusion increases and, although the same amount of solute molecules is depicted, these become locally more concentrated, i.e., their chemical potential has increased. As a consequence, to achieve thermodynamic equilibrium, the unfolding reaction is displaced to the native state, hence the solute acts as a stabilizer.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Figure 9.
Fluorescence decay times of staphylococcal nuclease as a function of temperature in the presence of 0.5 M mannosylglycerate (solid symbols) and in the absence of solutes (open symbols). Native protein: triangles; denatured states of the protein: squares and circles.
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10.1128/9781555815813/f0100-01.gif
Image of Figure 9.
Figure 9.

Fluorescence decay times of staphylococcal nuclease as a function of temperature in the presence of 0.5 M mannosylglycerate (solid symbols) and in the absence of solutes (open symbols). Native protein: triangles; denatured states of the protein: squares and circles.

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
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Tables

The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles
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Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
/content/10.1128/9781555815813.ch07.ch07tab01
Table 1.
Distribution of compatible solutes of (hyper)thermophilic microorganisms
Generic image for table
Table 1.

Distribution of compatible solutes of (hyper)thermophilic microorganisms

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7
/content/10.1128/9781555815813.ch07.ch07tab02
Table 2.
Biochemical properties of recombinant mannosyl-3-phosphoglycerate synthase from and
Generic image for table
Table 2.

Biochemical properties of recombinant mannosyl-3-phosphoglycerate synthase from and

Citation: Santos H, Lamosa P, Faria T, Borges N, Neves C. 2007. The Physiological Role, Biosynthesis, and Mode of Action of Compatible Solutes from (Hyper)Thermophiles, p 86-103. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch7

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