The maltodextrin system of Escherichia coli: glycogen-derived endogenous induction and osmoregulation

Abstract

Strains of Escherichia coli lacking MalQ (maltodextrin glucanotransferase or amylomaltase) are endogenously induced for the maltose regulon by maltotriose that is derived from the degradation of glycogen (glycogen-dependent endogenous induction). A high level of induction was dependent on the presence of MalP, maltodextrin phosphorylase, while expression was counteracted by MalZ, maltodextrin glucosidase. Glycogen-derived endogenous induction was sensitive to high osmolarity. This osmodependence was caused by MalZ. malZ, the gene encoding this enzyme, was found to be induced by high osmolarity even in the absence of MalT, the central regulator of all mal genes. The osmodependent expression of malZ was neither RpoS nor OmpR dependent. In contrast, the malPQ operon, whose expression was also increased at a high osmolarity, was partially dependent on RpoS. In the absence of glycogen, residual endogenous induction of the mal genes that is sensitive to increasing osmolarity can still be observed. This glycogen-independent endogenous induction is not understood, and it is not affected by altering the expression of MalP, MalQ, and MalZ. In particular, its independence from MalZ suggests that the responsible inducer is not maltotriose.

FIG. 1.

Enzymatic function of MalQ, MalZ, and MalP. Numbers give the approximate stoichiometry in the MalQ-catalyzed formation of the different maltodextrins when derived from maltose under equilibrium conditions (see accompanying publication [13]). Circles indicate glucosyl residues, with the arrows showing the reducing end. The action of MalP is the sequential formation of glucose-1-P from maltodextrins larger than maltotriose; the action of MalZ is the sequential formation of glucose from maltodextrins larger than maltose. Note that the final product of MalZ on any maltodextrin is maltose, whereas the final product of MalP is maltotriose. Not shown is that glucose and glucose-1-P enter glycolysis after their transformation to glucose-6-P by glucokinase and phosphoglucomutase, respectively.

FIG. 2.

Expression of malK-lacZ in isogenic strains differing in the presence or absence of MalQ (amylomaltase), MalP (maltodextrin phosphorylase), MalZ (maltodextrin glucosidase), and glycogen. Each strain was grown overnight in MMA with glycerol as the carbon source and, in addition, 0, 50, 100, 150, 200, 250, and 300 mM NaCl (from left to right for each of the 10 strains). The phenotype of each strain is shown underneath the groups of graphs for each strain and is given in a one-letter code, as follows: Q, MalQ; Z, MalZ; P, MalP; A, glycogen. Strains lacking glycogen are carrying a null mutation in glgA (encoding glycogen synthase).

FIG. 3.

Model of glycogen degradation and maltodextrin metabolism. The model of glycogen degradation as adapted from Dauvillée et al. (9). The distances between the branch points on one linear chain are not to scale but are much larger in vivo. The scheme includes the formation from glycogen of phosphorylase-limited glycogen by GlgP and the formation of maltotetraose by GlgX, the debranching enzyme. In the lower part, formation by MalP of maltotriose, the inducer of the maltose system (boxed), and the action of MalZ in removing maltotriose and the formation of maltose are shown. The glucosyl residues are indicated by circles, the α(1-4) linkage by the linear circle connector, and the reducing end by a straight arrow. The α(1-6) linkage is indicated by an angled arrow. The filled circles help to identify the origin of maltotriose.