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

• Published in: Journal of Bacteriology 2013-03, Vol.195 (5), p.1031-1041
• Main Authors: Linke, Caroline M, Woodiga, Shireen A, Meyers, Dustin J, Buckwalter, Carolyn M, Salhi, Hussam E, King, Samantha J
• Format: Article
• Language: English
• Subjects: ABC transporters; Adenosine triphosphatase; adenosinetriphosphatase; ATP-Binding Cassette Transporters - genetics; ATP-Binding Cassette Transporters - metabolism; bacteria; Bacteriology; beta-Fructofuranosidase - genetics; beta-Fructofuranosidase - metabolism; Biochemistry; Biological Transport - genetics; Carbohydrate Metabolism - genetics; Carbohydrates; fructose; Gene Expression Regulation, Bacterial; genes; Genetics; glucose; humans; inulin; Inulin - metabolism; kestose; loci; Oligosaccharides - chemistry; Oligosaccharides - metabolism; pathogens; Streptococcus infections; Streptococcus pneumoniae; Streptococcus pneumoniae - enzymology; Streptococcus pneumoniae - genetics; Streptococcus pneumoniae - metabolism; sucrose
• ISSN: 0021-9193; 1098-5530; 1067-8832
• DOI: 10.1128/JB.01560-12

Streptococcus 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 β-fructosidase (SP_1795) are required for utilization of several fructooligosaccharides longer than kestose, which consists of two β(2-1)-linked fructose molecules with a terminal α(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.