The Maltodextrin System ofEscherichia 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. Glycogenderived 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.The Escherichia coli maltodextrin system has become a paradigm for the understanding of a complex sugar-utilizing system in bacteria (3, 33). The regulon, controlled by MalT, the central activator of the system, consists of 10 coordinately regulated genes that are geared for the utilization of maltose and maltodextrins (for a detailed description of the different aspects of transport, enzymatic activity, and regulation, see the introduction of the accompanying publication [13]).One of the less clear phenomena in maltose regulation is endogenous induction. The degradation of glycogen yields maltodextrins which are channeled back into metabolism by MalQ and MalP (Fig. 1). Among these dextrins is maltotriose. In the absence of MalQ, maltotriose is no longer channeled into metabolism and is therefore able to activate MalT (14). This is the reason why malQ strains appear constitutive (12). We will refer to this type of endogenous induction as glycogenderived endogenous induction. However, even in strains lacking glycogen, the maltose system can be induced internally by growing the cells on carbon sources that yield internal glucose and ␣-glucose-1-phosphate (glucose-1-P) or glucose-6-P. For instance, the metabolism of trehalose is notorious for this production of internal inducer (11,22). It remains unclear whether the active inducer formed under these conditions is in fact maltotriose. Glycogen-independent induction will not be dealt with in this publication.In the absence of MalK, which is the major inhibiting factor of MalT (and which is counteracted by maltotriose) (20, 29), endogenous induction can most easily be recognized since little endogenous inducer is necessary under these conditions. Thus, even cultures grown in glycerol, which is known to cause catabolite repression (15, 16), are c...

The glgX gene product of Corynebacterium glutamicum is required for glycogen degradation and for fast adaptation to hyperosmotic stress

“…These phosphorylase-limit dextrins serve as substrates for the glycogen-debranching enzyme (Dauvillée et al, 2005). After debranching, the resulting linear maltodextrins serve as substrates for maltodextrin phosphorylase, which forms glucose 1-phosphate, and for maltodextrin glucosidase, which forms glucose (Dippel et al, 2005). None of these enzymes has been experimentally identified in C. glutamicum, although two genes in the genome (cg1479 and cg2289) have been annotated as glycogen phosphorylase genes, and a further gene (cg2310) has been annotated as glgX and putatively encodes a glycogen-debranching enzyme (Kalinowski et al, 2003).…”

Roles of maltodextrin and glycogen phosphorylases in maltose utilization and glycogen metabolism in Corynebacterium glutamicum

“…1). This enzyme catalyses the transfer of maltosyl and longer dextrinyl residues from intracellular maltodextrins such as maltotriose onto the maltose, which is taken up by a high-affinity binding-protein-dependent ABC transporter (Dippel et al, 2005;Daus et al, 2006;Chen et al, 2003). Thereby, MalQ forms larger maltodextrins and releases glucose (see Fig.…”

“…Glycogen phosphorylase (GlgP) cleaves a-1,4-glycosidic bonds at the non-reducing ends of glycogen and forms glucose 1-phosphate and phosphorylase-limited dextrins (pl-dextrins) (Dauvillee et al, 2005;Alonso-Casajus et al, 2006). Cleavage of the a-1,6-glycosidic bonds by the debranching enzyme GlgX leads to the formation of maltodextrins, which are then further degraded by maltodextrin phosphorylase (MalP) and maltodextrin glucosidase (MalZ) (Dippel et al, 2005). MalP and MalZ are also involved in maltose metabolism in E. coli, since in the course of maltose utilization, various maltodextrins are formed by 4-a-glucanotransferase (MalQ; see Fig.…”

Transcription of malP is subject to phosphotransferase system-dependent regulation in Corynebacterium glutamicum

“…At the onset of the stationary phase, when the initially provided glycolytic substrate has been consumed and the transiently accumulated glycogen has been degraded, malP transcript levels and MalP activity decrease (Clermont et al, 2015). In contrast to the situation in E. coli, in which malP transcription is activated via the transcriptional activator MalT by glycogen degradation products in the course of cultivation with glucose (Dippel et al, 2005;Ehrmann & Boos, 1987), activation of malP transcription occurs in C. glutamicum in cultivations on glycolytic substrates independent of the glycogen formation (Clermont et al, 2015). Based on the here observed interconnection between a functional PTS and control of malP transcription and the previously observed carbon-source-dependent regulation of malP transcription, it is tempting to speculate that the phosphorylation status of PTS components might act as a stimulus for the activation of malP transcription.…”