MalE of Group A Streptococcus Participates in the Rapid Transport of Maltotriose and Longer Maltodextrins

Abstract

Study of the maltose/maltodextrin binding protein MalE in Escherichia coli has resulted in fundamental insights into the molecular mechanisms of microbial transport. Whether gram-positive bacteria employ a similar pathway for maltodextrin transport is unclear. The maltodextrin binding protein MalE has previously been shown to be key to the ability of group A Streptococcus (GAS) to colonize the oropharynx, the major site of GAS infection in humans. Here we used a multifaceted approach to elucidate the function and binding characteristics of GAS MalE. We found that GAS MalE is a central part of a highly efficient maltodextrin transport system capable of transporting linear maltodextrins that are up to at least seven glucose molecules long. Of the carbohydrates tested, GAS MalE had the highest affinity for maltotriose, a major breakdown product of starch in the human oropharynx. The thermodynamics and fluorescence changes induced by GAS MalE-maltodextrin binding were essentially opposite those reported for E. coli MalE. Moreover, unlike E. coli MalE, GAS MalE exhibited no specific binding of maltose or cyclic maltodextrins. Our data show that GAS developed a transport system optimized for linear maltodextrins longer than two glucose molecules that has several key differences from its well-studied E. coli counterpart.Analysis of microbial carbohydrate physiology has been a fertile area of scientific research for many decades. Fundamental discoveries in the areas of transcriptional regulation, selective nutrient utilization, and molecular transport have been derived from studies of microbial carbohydrate acquisition and processing (13,27,34). For example, the uptake and utilization of maltose/maltodextrins by Escherichia coli has become a model for understanding how microbes transport and use complex sugars (3).The study of E. coli MalE, the periplasmic substrate binding protein of the maltose/maltodextrin ATP binding cassette transporter, has been a particularly fruitful area of investigation (32, 33). Although E. coli MalE binds to a variety of ␣-1,4-linked oligoglucosides, including linear, cyclic, reduced, and oxidized maltodextrins, only a portion of the bound ligands is subsequently transported into the cell (10). The interaction of purified E. coli MalE with the actively transported substrates maltose and maltotriose causes an increase in the E. coli MalE maximum emission wavelength (10, 39). The change in the fluorescence emission spectrum correlates with the closed and open forms of the E. coli . The closed form is needed for active transport to occur (11). The binding of E. coli MalE to substrates that are actively transported results in an endothermic reaction that is entropy driven (40). Conversely, the binding of E. coli MalE to nontransported substrates is exothermic and results in a decrease in the maximum fluorescence emission wavelength of E. coli MalE (9, 40). Therefore, study of E. coli MalE has generated data showing two major modes of ligand binding: one in which an endothermic reaction driven by...

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“…Growth defects on maltose and glucose were not found in our study likely due to the presence of non-PTS uptake systems. Transport of maltose in GAS has been shown to occur through both the MalE-dependent ABC transport system as well as the MalT-specific PTS pathway (49,50). In Lactococcus lactis, a non-PTS glucose uptake system (GlcU) has been reported; however, genes encoding a homologous system have not yet been identified in the genomes of S. pyogenes or S. pneumoniae (51).…”

Two Closely Related ABC Transporters in Streptococcus mutans Are Involved in Disaccharide and/or Oligosaccharide Uptake

“…A Streptococcus pneumoniae malX mutant, which lacks the CUT1 ABC transporter solute binding protein MalX, can no longer grow on maltotetraose as a sole carbon source but can grow on maltose (25). Similarly, a solute binding protein from Streptococcus pyogenes, MalE, is involved in the transport of linear maltodextrins with as many as 7 glucose units, but it does not bind maltose or cyclic maltodextrins (34). Therefore, the uptake of maltodextrins by ABC transporters of the CUT1 subfamily is common in Streptococcus species.…”

Effects of the ERES Pathogenicity Region Regulator Ralp3 on Streptococcus pyogenes Serotype M49 Virulence Factor Expression

“…GAS, as one of the major pathogenic lactic acid bacteria, utilizes glucose as a main carbon source (40). GAS glycolysis has recently been studied by a systems biology approach, and the first GAS glycolytic kinetic model has been published (23).Different transcriptomic studies have shown that virulence regulation by GAS is linked to genes that are important for sugar utilization (24,25,36,38). In particular, starch-degrading and carbohydrate-metabolism genes are differentially regulated during GAS stationary-phase survival in saliva (37).…”

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