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Chapter 11 : Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution

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Abstract:

Regulation of enzyme (levanase) and of an extra cellular fructosyltransferase (levansucrase [Lvs]) are reviewed in this chapter. Carbohydrate catabolism in other gram-positive bacteria is in most cases less well documented than that in . Catabolism of L-arabinose, D-xylose, sucrose, glycerol, and gluconate and the corresponding regulons are described in this chapter. Several gram-positive bacteria are able to catabolize lactose by means of diverse pathways. It has been known for decades that catabolic pathways are conserved elements in prokaryotes and more generally throughout all groups of living organisms. Three unique carbohydrate pathways in gram-positive bacteria have been highlighted here: pathways for glucitol and fructose utilization in and the tagatose-phosphate pathway for lactose-galactose degradation in and some lactic acid bacteria. The tagatose-phosphate pathway is a radical alternative to the otherwise ubiquitous Leloir galactose pathway. It is not known which of these pathways is t h e more recent innovation. species and have functional Leloir pathways , and other grampositive bacteria, including and , appear t o possess elements of this pathway. The diversity is such that it is impossible to define a typically gram-positive pattern of carbohydrate catabolism.

Citation: Steinmetz M. 1993. Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution, p 157-170. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch11

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Figure 1

Catabolism of hexoses, linear hexitols, and sucrose in Transport and enzymatic steps are symbolized by arrows. The names of the structural genes (in some cases putative) of the relevant proteins are indicated in italics and ). All these genes are both mapped (except for phosphoglucoisomerase) and inducible (except and ). Various controls prevent (or reduce) simultaneous expression of alternative pathways for sucrose and fructose (see text). Transfructosylation from sucrose by Lvs results mainly in a mixture of glucose, fructose, and levan. encodes levanase. Fra, Glu, Gut, Md, and Suc: fructose, glucose, glucitol, mannitol, and sucrose, respectively; Suc-P, sucrose-phosphate (phosphorylated on position 6 of glucose moiety). Other sugar-phosphates are designated according to standard conventions; for example, Glu-6-P and Fru-l,6-dP designate glucose 6-phosphate and fructose 1,6-diphosphate.

Citation: Steinmetz M. 1993. Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution, p 157-170. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch11
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Image of Figure 2
Figure 2

Organization of the gluconate operon and the xyloside-xylose regulon in The repressor of the operon is encoded by the first gene of the operon; and -Z very likely encode gluconate kinase, gluconate permease, and 6-phosphogluconate dehydrogenase, respectively; is transcribed from both the GntR-repressed promoter and a constitutive promoter within The repressor of the xylose-xyloside regulon (XylR) controls transcription of the and opérons; XynB is a xylosidase; XynC appears to be a membrane protein that might be a permease of xyloside and/or xylose; and and encode xylose isomerase and xylulose kinase, respectively. t, terminator.

Citation: Steinmetz M. 1993. Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution, p 157-170. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch11
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Figure 4

Regulons dependent on antiterminators and/or PTS control: comparison of regulation and genetic organization. The first three systems (a, b, and c) involve elements both structurally and functionally homologous: antiterminators, conditional terminators (ct), and enzymes II. (a) β-glucoside operon model. In the absence of β-glucoside inducer, transcription of the operon from the promoter is prevented by two conditional terminators bracketing the antiterminator gene. In these conditions, BglG function is inhibited by phosphorylation by the gene product (enzyme II). The presence of β-glucoside in the medium results in its transport and phosphorylation by enzyme II. This results in phosphate group rerouting. Dephosphorylated antiterminator then allows full transcription of the operon. BglB is the phospho-β-glucosidase ( ). (b) (Lvs) regulon. This regulon comprises the gene and the unlinked regulator operon. Both appear to be controlled by means of a regulatory cascade similar to that of the operon, i.e., positively by both sucrose and SacY antiterminator and negatively by SacX, a putative enzyme II. Several regulatory cross-talks with the regulon (see below) are not shown. The genes (DEG; see chapter 50) activate transcription from both and promoters ( ). (c) operon. Transcription of this operon is positively controlled by sucrose and the antiterminator encoded by the linked gene; appears not to play a role in this regulation ( ). The mechanism of SacT activation by the presence of sucrose is unknown (see text), (d) levanase operon. The first four genes encode an enzyme II (very poorly related to those mentioned above) controlling the LevR positive regulator. The fructose-dependent induction cascade appears similar to that of the operon but appears not to involve antitermination. LevR is a transcriptional activator binding upstream from the operon promoter and requiring σ as a cofactor ( ). (e) glycerol regulon. This regulon comprises at least two unlinked gene clusters and three promoters likely controlled by the gene product. This regulator (unrelated to BglG) appears to function as an antiterminator at conditional terminators just upstream from and ( ).

Citation: Steinmetz M. 1993. Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution, p 157-170. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch11
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Figure 3

Sucrose gene clusters in four bacteria. The comparison includes two gram-positive systems, from and and two gram-negative systems (sucrose operon in a close relative of enteric bacteria, and sucrose genes present on the pUR400 plasmid; the pUR400 sucrose regulon appears to be closely related to the chromosomal sucrose system). The four enzymes nsucrose, encoded by (in ) or genes, are structurally homologous. The ScrA protein contains a C-terminal extension containing a second phosphorylation site (enzyme III domain). The gene designated in or in and encodes related phosphosucrases (the pUR400 gene sequence is unknown). Expression of the sucrose genes is stimulated by the presence of different sugars in the medium (see text). The three other systems are specifically induced by sucrose via activation of the SacT antiterminator in or inactivation of ScrR repressors in the case of the pUR400 or systems. The two ScrR repressors are not strongly similar, but both belong to the LacI-GalR superfamily; the pUR400-encoded ScrR repressor binds fructose; the two gram-negative regulons are dependent on the cyclic-AMP receptor protein-cyclic-AMP complex. The and genes encode fructokinase and a sucrose porin (related to the LamB maltoporin), respectively, encodes unknown functions (probably not involved in sucrose metabolism) (see references , and and references therein). The sucrose genes were recendy cloned and sequenced; the gene products are homologous to those mentioned above. (encoding a short enzyme II) and are unlinked. Both are sucrose inducible via a negative control. Similar operatorlike sequences are found in both leader regions ( ).

Citation: Steinmetz M. 1993. Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution, p 157-170. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch11
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Figure 5

FTS-dependent lactose systems of and some lactic acid-producing bacteria: pathways and gene organization. (A) Transport and catabolism of lactose via the tagatose 6-phosphate pathway. Lactose is transported and phosphorylated by enzyme II (II) and then hydrolyzed into glucose (catabolized by the classical glycolysis pathway) and Gal-6-P, which is isomerized to tagatose 6-phosphate (Tag-6-P). Tag-6-P is converted, by means of a pathway similar to that of its isomer, fructose 6-phosphate (Fru-6-P), into two molecules of triose-phosphate (dihydroxyacetone-phosphate [DHA-P] and glyceraldehyde 3-phosphate [GA-3-P]) and then into phosphoenolpyru-vate (PEP). Dephosphorylation of PEP to pyruvate results partly in ATP production (not shown) and partly in phosphorylation of proteins of the cytoplasmic PTS cascade. This cascade ends with phosphorylation of the membrane enzyme II protein by the cytoplasmic enzyme III (III) protein. In lactic acid bacteria, lactate produced from pyruvate is excreted with protons; this-coexcretion contributes to energizing the proton motive force. A, H, I, and K, aldolases, hydrolases, isomerases, and kinases, respectively. The genes encoding the enzymes of the pathway are indicated in parentheses. (B) Organization of the opérons in and Arrows indicate the transcripts; t, t1, and t2 are transcriptional terminators. Three major features distinguish the operon from that of the orientation of the gene, the presence of a weak terminator (tl) downstream from and the presence of an eighth gene, of unknown function, at the 3′ end of the operon. The 5′ end of the operon has not yet been sequenced, but its transcript is similar in size to that of (Adapted from references , and )

Citation: Steinmetz M. 1993. Carbohydrate Catabolism: Pathways, Enzymes, Genetic Regulation, and Evolution, p 157-170. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch11
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