The ABC Transporter Encoded at the Pneumococcal Fructooligosaccharide Utilization Locus Determines the Ability To Utilize Long- and Short-Chain Fructooligosaccharides

Abstract

bStreptococcus pneumoniae is an important human pathogen that requires carbohydrates for growth. The significance of carbohydrate acquisition is highlighted by the genome encoding more than 27 predicted carbohydrate transporters. It has long been known that about 60% of pneumococci could utilize the fructooligosaccharide inulin as a carbohydrate source, but the mechanism of utilization was unknown. Here we demonstrate that a predicted sucrose utilization locus is actually a fructooligosaccharide utilization locus and imparts the ability of pneumococci to utilize inulin. Genes in strain TIGR4 predicted to encode an ABC transporter (SP_1796-8) and a ␤-fructosidase (SP_1795) are required for utilization of several fructooligosaccharides longer than kestose, which consists of two ␤(2-1)-linked fructose molecules with a terminal ␣(1-2)-linked glucose molecule. Similar to other characterized pneumococcal carbohydrate utilization transporter family 1 transporters, growth is dependent on the gene encoding the ATPase MsmK. While the majority of pneumococcal strains encode SP_1796-8 at this genomic location, 19% encode an alternative transporter. Although strains encoding either transporter can utilize short-chain fructooligosaccharides for growth, only strains encoding SP_1796-8 can utilize inulin. Exchange of genes encoding the SP_1796-8 transporter for those encoding the alternative transporter resulted in a TIGR4 strain that could utilize short-chain fructooligosaccharide but not inulin. These data demonstrate that the transporter encoded at this locus determines the ability of the bacteria to utilize long-chain fructooligosaccharides and explains the variation in inulin utilization between pneumococcal strains.

Sialic Acid-Mediated Gene Expression in Streptococcus pneumoniae and Role of NanR as a Transcriptional Activator of the nan Gene Cluster

“…For survival in the host, bacteria rely not only on the different virulence factors they possess but also on the appropriate use of nutrients available in their habitat (4,5). The ability of S. pneumoniae to utilize a variety of carbohydrate sources is one of the crucial factors in successful colonization and in causing pneumococcal infections (6). Metabolic selection enables a bacterium to choose a preferred source of carbon over a nonpreferred one through a mechanism called carbon catabolite repression (CCR) (5).…”

Structural Basis for Regulation and Specificity of Fructooligosaccharide Import in Streptococcus pneumoniae

“…A transporter mutant had a mild phenotype in the lung, but any role in colonization was not examined. Subsequent data revealed that this transporter does not contribute to sucrose utilization, but transports fructooligosaccharides (FOSs) including inulin and as a result was renamed the Fus (FOS utilization system) transporter (Linke et al., 2013). FOSs consist of a variable number (n) of D-fructose units linked by β2-1 bonds and a terminal D-glucose connected through an α2-1 bond.…”

“…While the majority of pneumococcal strains can utilize long-chain FOSs as a sole carbon source, some strains are only able to grow on shorter chain FOSs (Bidossi et al., 2012, Langvad-Nielsen, 1944, Linke et al., 2013, Morch-Lund, 1949). Examination of 33 clinical isolates demonstrated that all six strains that were able to use GF3 but not inulin as a sole carbon source encoded an alternative transporter named Sfu (short-chain FOS utilization) (Linke et al., 2013). The SBP of this transporter shares little sequence similarity with that encoded by the fus locus and the structural basis of the substrate specificity is unclear.…”

N-acetylglucosamine-Mediated Expression of nagA and nagB in Streptococcus pneumoniae

“…The deglycosylation activity of both exo- and endoglycosidades has previously been demonstrated in S. pneumoniae (King et al, 2006; Burnaugh et al, 2008; Jeong et al, 2009; Marion et al, 2009). The ability to utilize complex glycans present at the site of colonization contributes to the successful survival and virulence of S. pneumoniae in the host (Buckwalter and King, 2012; Linke et al, 2013). Besides, the role of these enzymes in in vivo fitness is demonstrated by the findings that glycosidase mutants show attenuated capacity to colonize and to cause disease in mouse models (Tong et al, 2000; Jeong et al, 2009; Marion et al, 2009; Terra et al, 2010).…”