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Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation - PubMed

Review

Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation

Christopher Bräsen et al. Microbiol Mol Biol Rev. 2014 Mar.

Abstract

The metabolism of Archaea, the third domain of life, resembles in its complexity those of Bacteria and lower Eukarya. However, this metabolic complexity in Archaea is accompanied by the absence of many "classical" pathways, particularly in central carbohydrate metabolism. Instead, Archaea are characterized by the presence of unique, modified variants of classical pathways such as the Embden-Meyerhof-Parnas (EMP) pathway and the Entner-Doudoroff (ED) pathway. The pentose phosphate pathway is only partly present (if at all), and pentose degradation also significantly differs from that known for bacterial model organisms. These modifications are accompanied by the invention of "new," unusual enzymes which cause fundamental consequences for the underlying regulatory principles, and classical allosteric regulation sites well established in Bacteria and Eukarya are lost. The aim of this review is to present the current understanding of central carbohydrate metabolic pathways and their regulation in Archaea. In order to give an overview of their complexity, pathway modifications are discussed with respect to unusual archaeal biocatalysts, their structural and mechanistic characteristics, and their regulatory properties in comparison to their classic counterparts from Bacteria and Eukarya. Furthermore, an overview focusing on hexose metabolic, i.e., glycolytic as well as gluconeogenic, pathways identified in archaeal model organisms is given. Their energy gain is discussed, and new insights into different levels of regulation that have been observed so far, including the transcript and protein levels (e.g., gene regulation, known transcription regulators, and posttranslational modification via reversible protein phosphorylation), are presented.

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Figures

FIG 1
FIG 1

Glucose degradation via the EMP pathway known for most Bacteria and Eukarya (classical) and the modified EMP versions reported for Archaea. Allosterically regulated enzymes are depicted in red. Abbreviations: ENO, enolase; FBPA, fructose-1,6-bisphosphate aldolase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; GAPN, nonphosphorylating GAPDH; GAPOR, GAP:Fd oxidoreductase; GLK, glucose kinase; HK, hexokinase; PEPS, PEP synthetase; PFK, phosphofructokinase; PGI, phosphoglucose isomerase; PGI/PMI, phosphoglucose isomerase/phosphomannose isomerase; cPGI, cupin-type phosphoglucose isomerase; PGAM, phosphoglycerate mutase (dPGAM, 2,3-bisphosphoglycerate [2,3BPG] cofactor dependent; iPGAM, 2,3BPG cofactor independent); PK, pyruvate kinase; PPDK, pyruvate:phosphate dikinase; ROK, hexokinase of the repressor protein, open reading frame, sugar kinase family; G6P, glucose 6-phosphate; F6P, fructose 6-phosphate; F1,6BP, fructose 1,6-bisphosphate; DHAP, dihydroxyacetone phosphate; GAP, glyceraldehyde 3-phosphate; 1,3BPG, 1,3-bisphosphoglycerate; 3PG, 3-phosphoglycerate; 2PG, 2-phosphoglycerate; PEP, phosphoenolpyruvate.

FIG 2
FIG 2

Ribbon representation of the crystal structures of the monomers of the different sugar kinases found in Archaea. (A) ADP-GLK from Pyr. furiosus (PDB accession number 1UA4) (59) as a representative of the ADP-dependent sugar kinase family within the ribokinase superfamily also comprising ADP-PFKs as well as the promiscuous ADP-GLK/PFK from Mca. jannaschii. (B) KDGK from Sul. solfataricus (PDB accession number 2VAR) (122) as a member of the ribokinase superfamily, exhibiting the PFK-B fold like the ATP-dependent PFKs present in, e.g., Des. amylolyticus and Aer. pernix. (C) HK from Sul. tokodaii (PDB accession number 2E2N) (49) as a member of the actin-ATPase domain-like superfamily also comprising ROK hexokinases and classical HKs from Eukarya and Bacteria. (D) Classical phosphofructokinase from E. coli (PDB accession number 6PFK) (101) as a member of the PFK-A family, to which also the PPi-dependent PFK from Tpt. tenax belongs. All illustrations of crystal structures were prepared by using the Pymol Molecular Graphics System, version 1.3 (Schrödinger, LLC).

FIG 3
FIG 3

Proposed reaction mechanism catalyzed by sugar kinases, including base-mediated proton abstraction from the acceptor hydroxyl group followed by nucleophilic attack on the γ-phosphate group of ATP.

FIG 4
FIG 4

(A) Crystal structure of the monomer of PGI/PMI from Pyb. aerophilum (PDB accession number 1X9H) (87), which shows the PGI superfamily fold. Both PGI/PMIs and classical PGIs constitute distinct families within the PGI superfamily. (B) Monomer of cPGI from Pyr. furiosus (PDB accession number 2VAR) (96), which shows the small barrel formed by two β sheets, typical of the cupin superfamily.

FIG 5
FIG 5

Schemes illustrating the proposed reaction mechanisms for dehydratases, enolases, class II aldolases, and isomerases, all proceeding via an enediolate intermediate (highlighted by the box).

FIG 6
FIG 6

(A and B) Ribbon diagrams of the archaeal-type class I FBPA (PDB accession number 1OJX) (135) (A) and KD(P)GA (PDB accession number 2R91) (298) (B) from Tpt. tenax, both members of the class I aldolase family within the aldolase superfamily. (C) For comparison, the class II FBPA from E. coli is depicted (PDB accession number 1B57) (138), which also has been described for some halophilic Archaea. Class II aldolases constitute a distinct family within the aldolase superfamily. However, the figures show that all of these aldolases share a (β/α)8 TIM barrel fold.

FIG 7
FIG 7

Schiff base mechanism catalyzed by FBPAs and KD(P)GAs in the course of the modified sugar degradation pathways in Archaea. The first step is the nucleophilic attack of the catalytically essential lysine at the carbonyl C atom, yielding the carbinolamine intermediate, which is then dehydrated to the Schiff base, followed by base-mediated cleavage of the substrate. −H/OH means that in this position, the substituent is either a hydroxyl group (as in fructose converted by FBPA) or a hydrogen atom [as in 2-keto-3-deoxy sugar acids converted by KD(P)GA]. The bifunctional FBPA/ase from gluconeogenesis in Archaea catalyzes a similar reaction in the first part of the conversion of GAP and DHAP to F6P (for a more detailed discussion, see Gluconeogenesis, below).

FIG 8
FIG 8

Comparative illustrations of the classical triosephosphate isomerase (TIM) barrel fold present in TIM (here from T. tenax [PDB accession number 1W0M]) (147) and the modified ββαα(βα)6 barrel fold from the enolase superfamily members (here from the putative enolase of Mca. jannaschii [PDB accession number 2PA6]) (229), comprising, besides ENOs, dehydratases used in the degradation of hexoses and pentoses in Archaea (see Fig. 5 for the reaction mechanism of isomerases and enolases).

FIG 9
FIG 9

Ribbon representations of GAP-oxidizing enzymes in Archaea. (A) GAPN from Tpt. tenax (PDB accession number 1UXN) (174) showing the three-domain organization. GAPN is a member of the ALDH superfamily, also comprising the glyceraldehyde dehydrogenases from the npED branch in Thermoplasma spp. and α-ketoglutarate semialdehyde dehydrogenases from the pentose degradation pathway in Sulfolobus and Haloferax. (B) Aldehyde:ferredoxin oxidoreductase from Pyr. furiosus (PDB accession number 1AOR) (169), a representative of the AOR superfamily, to which the archaeal GAPORs also belong. The protein is organized in three domains, with the pterin cofactor and Fe/S cluster (depicted as a green stick model) binding site in the center between the three domains. (C) The classical GAPDH from Sul. solfataricus (PDB accession number 1B7G) (193) is shown operating exclusively in the anabolic/gluconeogenic direction, exhibiting the typical two-domain structure with an N-terminal Rossman fold nucleotide binding domain and a C-terminal catalytic domain.

FIG 10
FIG 10

Proposed catalytic mechanism of classical phosphorylating GAPDH and nonphosphorylating GAPN with similar first acylation and hydride transfer steps and different deacylation steps, with phosphate as the acyl acceptor in GAPDH and water as the acyl acceptor in GAPN.

FIG 11
FIG 11

PK monomer crystal structure from Pyb. aerophilum (PDB accession number 3QTG) (244) shown as a ribbon diagram. As for classical PKs, the archaeal enzyme exhibits a three-domain structure, with a central TIM barrel catalytic domain flanked on one side by the cap domain and on the other side by the allosteric domain, where effector binding takes place.

FIG 12
FIG 12

Glucose degradation via the Entner-Doudoroff (ED) pathways known for Bacteria (classical) and the modified branched versions reported for Archaea. The nonphosphorylative ED (npED) and the semiphosphorylative ED (spED) branches in Archaea, with phosphorylation at the level of glycerate and 2-keto-3-deoxygluconate (KDG), respectively, are shown. Abbreviations: 6PGD (EDD), gluconate-6-phosphate dehydratase; ENO, enolase; G6PDH (Zwf), glucose-6-phosphate dehydrogenase; GAD, gluconate dehydratase; GADH, glyceraldehyde dehydrogenase; GAOR, glyceraldehyde:ferredoxin oxidoreductase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; GAPN, nonphosphorylating GAPDH; GAPOR, GAP:Fd oxidoreductase; GDH, glucose dehydrogenase; GK, glycerate kinase; GLac, gluconolactonase; GLK, glucokinase; HK, hexokinase; KDGK, 2-keto-3-deoxygluconate kinase; KDPGA (EDA), 2-keto-3-deoxy-6-phosphogluconate aldolase; KD(P)GA, 2-keto-3-deoxy-(6-phospho)gluconate aldolase; PGK, phosphoglycerate kinase; PGL, 6-phosphoglucono-1,4-lactonase; PGAM, phosphoglycerate mutase (dPGAM, 2,3BPG cofactor dependent; iPGAM, 2,3BPG cofactor independent); PK, pyruvate kinase; PEPS, PEP synthetase; PPDK, pyruvate:phosphate dikinase; PTS, PEP-dependent phosphotransferase system; G6P, glucose 6-phosphate; GAP, glyceraldehyde 3-phosphate; 1,3BPG, 1,3-bisphosphoglycerate; 3PG, 3-phosphoglycerate; 2PG, 2-phosphoglycerate; PEP, phosphoenolpyruvate; KDG, 2-keto-3-deoxygluconate; KDPG, 2-keto-3-deoxy-6-phosphogluconate; GA, glyceraldehyde.

FIG 13
FIG 13

(A) Promiscuous GDH (PDB accession number 2CD9) (269) involved in hexose and pentose degradation in Sul. solfataricus exhibiting the typical two-domain dehydrogenase topology of the MDR superfamily members. (B) For comparison, the G6PDH structure from Leuconostoc mesenteroides (PDB accession number 1E7Y) (280), involved in the classical ED pathway, is shown. (C) The crystal structure of the Zymomonas mobilis glucose-fructose oxidoreductase is depicted (PDB accession number 1OFG) (349), which belongs to the same protein superfamily as the XDH described for Hfx. volcanii. For each protein, the ribbon representation of one monomer is shown.

FIG 14
FIG 14

(A) Crystal structure of the monomer of the bifunctional fructose-1,6-bisphosphate aldolase/phosphatase (class V phosphatase) (PDB accession number 3T2B) (342) bypassing the FBPA and PFK reactions in gluconeogenesis of most Archaea and deeply branching Bacteria. The bifunctional FBPA/ase exhibits an α-β-β-α four-layered sandwich fold. (B) However, the class I phosphatase from E. coli (PDB accession number 2OX3) (579) shows an α-β-α-β-α five-layered sandwich fold (similar to class II and class IV phosphatases). Class I phosphatase represents the canonical enzyme in gluconeogenesis of Eukarya and Bacteria.

FIG 15
FIG 15

(A) Pentose degradation pathway found in Bacteria and Eukarya (yeasts, mammals, and fungi), proceeding via isomerases (I), kinases (K), and epimerases (E). (B) In few Bacteria, pentose degradation proceeds via reductases (R), dehydrogenases (DH), and kinases (K).

FIG 16
FIG 16

Current understanding of pentose degradation pathways in Archaea. The degradation pathways reported for

d

-arabinose,

d

-xylose, and

l

-arabinose in Sulfolobus spp. (A) and the

d

-xylose degradation pathway in Haloferax volcanii (B) are depicted. The dashed arrow indicates the presence of lactones as intermediates, which are supposed to be spontaneously transformed to the respective sugar acid at high temperatures. AraDH,

d

-arabinose dehydrogenase; AraD,

d

-arabinoate dehydratase; α-KGSADH, α-ketoglutarate semialdehyde dehydrogenase; GDH-1, glucose dehydrogenase (isoenzyme 1) (SSO3003); GlyAlOR, glycolaldehyde:ferredoxin oxidoreductase; GlyDH, glycolate dehydrogenase; KD(P)G aldolase, 2-keto-3-deoxy-(6-phospho)gluconate aldolase; KDAD, 2-keto-3-deoxyarabinoate dehydratase; MS, malate synthase; KDXD, 2-keto-3-deoxyxylonate dehydratase; XDH, xylose dehydrogenase; XylLac, xylono-1,4-lactone lactonase;

d

-XAD, xylonate dehydratase.

FIG 17
FIG 17

Crystal structure of the KDAD monomer from Sul. solfataricus (PDB accession number 3QTG) (355) shown as a ribbon diagram. The enzyme consists of an N-terminal domain and a C-terminal catalytic domain and belongs to the fumarylacetoacetate hydrolase (FAH) superfamily.

FIG 18
FIG 18

Current understanding of pathways for pentose formation in the three domains of life. Depicted are the reversed ribulose monophosphate pathway, the nonoxidative pentose phosphate pathway, and the oxidative pentose phosphate pathway. Enzymes depicted in red have not been identified in Archaea so far. Abbreviations: G6PDH, glucose-6-phosphate dehydrogenase; 6PGL, 6-phosphogluconate-

d

-lactonase; 6PGDH 6-phosphogluconate dehydrogenase; RPI, ribose-5-phosphate isomerase; RPE, ribose-5-phosphate-3-epimerase; TK, transketolase; TA, transaldolase; HPS, 3-hexulose-6-phosphate synthase; PHI, 6-phospho-3-hexuloisomerase.

FIG 19
FIG 19

Erythrose 4-phosphate and pentose 5-phosphate synthesis via the incomplete NOPPP, as found in most archaea. All required building blocks, e.g., ribose 5-phosphate for nucleotides and erythrose 4-phosphate for aromatic amino acid synthesis, are formed. The fate of seduheptulose 7-phosphate is still unclear. Abbreviations: HPS, 3-hexulose-6-phosphate synthase; PHI, 6-phospho-3-hexuloisomerase; RPI, ribose-5-phosphate isomerase; TK, transketolase.

FIG 20
FIG 20

Glycolysis and gluconeogenesis in the anaerobic hyperthermophile Thermococcus kodakarensis. Tco. kodakarensis utilizes the reversible EMP pathway for glycolysis and gluconeogenesis. The glycolytic pathway is characterized by ADP-dependent sugar kinases, archaeal-type class I FBPA, catabolic irreversible GAPN and GAPOR, and reversible PEPS, besides PK, with preferred glycolytic function. In gluconeogenesis, besides PEPS, alternative reactions, such as those catalyzed by PCK, seem to contribute to PEPS formation. The anabolic direction is characterized by the anabolic PGK/GAPDH enzyme couple as well as FBPA/ase. Enzyme reactions with catabolic function are indicated by red arrows, anabolic reactions are indicated by blue arrows, and reversible reactions are shown as black arrows. Effectors are given in green and red boxes for activators and inhibitors, respectively. Genes comprising the TGM for binding of the transcriptional regulator Tgr (see also Fig. 21) are marked by a blue dot (TGM upstream of the BRE/TATA box, activator binding for genes encoding gluconeogenic proteins) or a red dot (TGM downstream of the BRE/TATA box, repressor binding for genes encoding glycolytic proteins) (208). Transcript levels of genes which are upregulated under glycolytic or gluconeogenic conditions are marked with red or blue open arrows, respectively (208). The net equations of glucose conversion to pyruvate via the modified EMP pathway with utilization of PEP synthetase (+PEPS) and pyruvate kinase (+PK) are indicated in boxes (GLGA, glycogen synthase; GLPG, glycogen phosphorylase; AMYA, α-amylase; PCK, PEP carboxykinase; PGM, phosphoglucomutase; AK, adenylate kinase). (Electron micrograph courtesy of Haruyuki Atomi, Kyoto University, Japan, reproduced with permission.)

FIG 21
FIG 21

Gene clusters encoding the trehalose/maltose (TM) and maltodextrin (MD) ABC transporters in Tco. kodakarensis and Pyr. furiosus. Whereas Pyr. furiosus possesses the TM and MD systems (481), Tco. kodakarensis possesses only the MD system (208) and is not able to utilize maltose or trehalose as a carbon source. In Tco. kodakarensis, the gene encoding the Thermococcales glycolytic regulator (Tgr; TK1769) is positioned divergently from the gene cluster comprising components of the ABC transporter (i.e., substrate binding protein [TK1771], two permeases [TK1772 and TK1773], and ATP binding protein [TK1775]), and genes encoding enzymes involved in polymer degradation (i.e., amylopullulanase [TK1774] and cyclomaltodextrinase [TK1770]). The TM gene cluster of Pyr. furiosus possesses, besides the genes encoding the ABC transporter components, genes encoding fructokinase (PF1738) (divergently oriented), trehalose synthase (TreT; PF1742 involved in trehalose utilization), and the transcriptional regulator TrmB (PF1743). The Pyr. furiosus MD gene cluster is also comprised of genes encoding enzymes involved in polymer degradation (i.e., α-amylase [PF1939] and amylopullulanase [PF1935]) and a hypothetical protein (PF1934). Components of the ABC transporter are depicted in gray, enzymes involved in sugar degradation are shown in orange, hypothetical proteins are shown in yellow, and transcriptional regulators are depicted in red.

FIG 22
FIG 22

Model for the function of the Thermococcales glycolytic regulator (Tgr) in differential expression of glycolytic and gluconeogenic genes in Tco. kodakarensis (208). Tgr serves as a repressor for glycolytic genes (Thermococcales glycolytic motif [TGM] located downstream of the promoter element [BRE/TATA]) and as an activator for gluconeogenic genes (TGM upstream of the promoter element). (A) Under gluconeogenic growth conditions (absence of the effector maltotriose), Tgr binds to the TGM, inhibits transcription of glycolytic genes, and activates transcription of gluconeogenic genes. (B) Under glycolytic growth conditions, in the presence of the effector (maltotriose) binding of Tgr to DNA is relieved. Abbreviations: RNAP, RNA polymerase; TFB, transcription factor B; TBP, TATA binding protein; BRE, TFB-responsive element; TATA, TATA box; ATG, start codon.

FIG 23
FIG 23

Model for TrmB and TrmBL1 function in differential regulation of genes encoding enzymes catalyzing transport, glycolysis, and gluconeogenesis in Pyr. furiosus. Under in vivo conditions, the cellular glucose concentration is supposed to be the major regulatory signal (482). (A) At high cellular glucose concentrations, autorepression of the gene encoding TrmBL1 is released, and TrmBL1 is present in high concentrations. High cellular concentrations of TrmBL1 inducers (i.e., maltose and maltotriose) will cause a shift from the tetrameric regulator (inducer sensitive) to the octameric regulator (not responsive to inducers) with high DNA binding affinity. In addition, glucose serves as a corepressor for TrmB, repressing the TM and MD systems. For many promoters tested, cross-regulation was observed for TrmBL1 and TrmB. In general, high cellular glucose concentrations lead to the repression of genes involved in glycolysis and transport (TM and MD systems) and activation of gluconeogenic genes. (B) At low cellular glucose concentrations, TrmBL1 expression is repressed, and low concentrations of the inducers maltose and maltotriose result in the formation of the inducer-responsive tetrameric form of TrmBL1 with a low DNA binding capacity. TrmB repression of the MD system is relieved by maltotriose, maltodextrin, or sucrose (maltose serves as a corepressor), and that of the TM system is relieved by trehalose and maltose, thus enhancing sugar uptake. Therefore, at low cellular glucose concentrations, expression of genes involved in transport (TM and MD systems) and glycolytic genes will be stimulated, whereas the expression of genes involved in gluconeogenic genes will be reduced.

FIG 24
FIG 24

Glycolysis and gluconeogenesis in the aerobic thermoacidophile Sulfolobus solfataricus. Sul. solfataricus utilizes the branched ED pathway for

d

-glucose and

d

-galactose degradation. Gluconeogenesis proceeds via the EMP pathway; for functional glycolysis, only PFK is missing. The ED pathway is characterized by promiscuous enzymes for glucose and galactose degradation up to the level of aldol cleavage. The spED branch is characterized by KDGK, glycolytic, allosterically regulated GAPN, and glycolytic PK, and the npED branch is characterized by GK, which shows substrate inhibition. For gluconeogenesis, the EMP pathway utilizes PEPS, the PGK/GAPDH enzyme couple, as well as FBPA/ase, with PGK and TIM being allosterically regulated. Enzyme reactions with catabolic function are indicated by red arrows, anabolic reactions are indicated by blue arrows, and reversible reactions are indicated by black arrows. Effectors are given in green and red boxes for activators and inhibitors, respectively. Enzymes identified as phosphoproteins under glycolytic (glucose) or gluconeogenic (tryptone) growth conditions are marked by black dots, with T for tryptone and G for glucose (439). Enzymes that were upregulated (>1.5-fold) at the protein level in response to glucose or complex medium (tryptone and yeast extract) are marked with red and blue open arrows, respectively (505). The net equation of glucose conversion to pyruvate via the branched ED pathway is depicted in the box (GLGA, glycogen synthase; GLPG, glycogen phosphorylase; AMYA, α-amylase; PGM, phosphoglucomutase). (Electron micrograph courtesy of Sonja-Verena Albers, Max Planck Institute, Marburg, Germany, reproduced with permission.)

FIG 25
FIG 25

Glycolysis and gluconeogenesis in the anaerobic hyperthermophile Thermoproteus tenax. Tpt. tenax utilizes both the reversible EMP and branched ED pathways for glycolysis and the EMP pathway for gluconeogenesis. The reversible EMP pathway is characterized by reversible PPi-PFK, catabolic GAPN and GAPOR, anabolic PGK-GAPDH, catabolic PK, anabolic PEPS, and a reversible PPDK with preferred glycolytic function. Enzyme reactions with catabolic function are indicated by red arrows, anabolic reactions are indicated by blue arrows, and reversible reactions are indicated by black arrows. Effectors are given in green and red boxes for activators and inhibitors, respectively. Enzymes for which the encoding genes were upregulated under heterotrophic/glycolytic (glucose) or autotrophic/gluconeogenic (CO2/H2) growth conditions are depicted as open red and blue arrows, respectively (31). The net equations of glucose conversion to pyruvate via the modified EMP pathway and the branched ED pathway are depicted in boxes (GLGA, glycogen synthase; GLPG, glycogen phosphorylase; AMYA, α-amylase; PGM, phosphoglucomutase). (Electron micrograph courtesy of Reinhard Rachel, University of Regensburg, Germany, reproduced with permission.)

FIG 26
FIG 26

Overview of fructose uptake by the PTS and degradation of fructose 1-phosphate in Hfx. volcanii (123). Fructose uptake proceeds via the PEP-dependent PTS; the different PTS components (EI, HPr, EIIA, EIIB, and EIIC) are depicted. The fructose 1-phosphate formed is further converted via fructose-1-phosphate kinase (1-PFK) (pfkB) and class II fructose-1,6-bisphosphate aldolase (FBPA) (fba), forming dihydroxyacetonephosphate (DHAP) and glyceraldehyde 3-phosphate (GAP). Abbreviations: PEP, phosphoenolpyruvate; CM, cytoplasmic membrane, ~P, transferred phosphate group.

FIG 27
FIG 27

Glycolysis and gluconeogenesis in the mesophilic halophile Haloferax volcanii. Glucose is degraded via the spED pathway, and fructose is degraded via the EMP pathway. The pathway for fructose degradation is characterized by 1-PFK and FBPA class II; the common lower EMP shunt is characterized by two GAPDH isoenzymes that are differently regulated in response to the C source (553) as well as catabolic PK and anabolic PEPS. Enzyme reactions with catabolic function are indicated by red arrows, anabolic reactions are shown as blue arrows, and reversible reactions are indicated by black arrows. Enzymes for which the encoding genes are regulated by the transcriptional regulator GlpR are marked (black box). Enzymes for which the encoding genes were up- or downregulated in response to the gluconeogenic (Casamino Acids)/glycolytic (glucose) shift are depicted as red open arrows in the respective direction (553). The net equations of glucose conversion to pyruvate via the modified ED pathway and of fructose conversion to pyruvate via the modified EMP pathway are depicted in boxes (PTS, PEP-dependent phosphotransferase system; KHK, ketohexokinase; 1-PFK, fructose-1-phosphate kinase). (Electron micrograph courtesy of Moshe Mevarech, Tel Aviv University, Israel, reproduced with permission.)

FIG 28
FIG 28

Genomic context of genes encoding components of the PEP-dependent phosphotransferase system (PTS) in Hfx. volcanii. Components of the fructose PTS system are colocalized with genes encoding the transcriptional regulator GlpR and enzymes involved in fructose 1-phosphate degradation, i.e., fructose-1-phosphate kinase and fructose-1,6-bisphosphate aldolase. Downstream of genes encoding enzymes for glycerol utilization (i.e., glycerol kinase and glycerol-3-phosphate dehydrogenase) forming dihydroxyacetone phosphate (DHAP), a gene encoding a second single Hpr2 and, in a divergent organization, genes encoding dihydroxyacetone kinase (dhaM, dhaL, and dhaK) are found. Hpr2 has been proposed to encode a cytosolic PTS complex, i.e., the dihydroxyacetone kinase (dhaM, dhaL, and dhaK) pathway, catalyzing the formation of DHAP from dihydroxyacetone (556). A second incomplete PTS gene cluster is found downstream of the gene encoding triosephosphate isomerase.

FIG 29
FIG 29

Glycolysis and gluconeogenesis in the autotrophic methanogens Methanococcus maripaludis and Methanocaldococcus jannaschii. The most extensively studied, Mco. maripaludis, for example, is a glycogen-forming methanogen and relies on the EMP pathway for glycolysis and gluconeogenesis. Glycolysis is characterized by a bifunctional ADP-GLK/PFK, archaeal-type class I FBPA, GAPOR, as well as PK, and gluconeogenesis is characterized by PEPS and FBPA/ase. The function of the GAPDH/PGK couple in gluconeogenesis and/or glycolysis still remains to be elucidated. Enzyme reactions with catabolic function are indicated by red arrows, anabolic reactions are indicated by blue arrows, and reversible reactions are indicated by black arrows. Effectors are given in green and red boxes for activators and inhibitors, respectively. The net equation of glucose 6-phosphate conversion to pyruvate via GAPDH/PGK or GAPOR in the modified EMP pathway is indicated in the box (GLGA, glycogen synthase; GLPG, glycogen phosphorylase; PGM, phosphoglucomutase; AK, adenylate kinase; 6PG, 6-phosphogluconate; E4P, erythrose 4-phosphate). (Electron micrograph courtesy of Reinhard Rachel, University of Regensburg, Germany, reproduced with permission.)

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