Extensive Identification of Bacterial Riboflavin Transporters and Their Distribution across Bacterial Species.
Riboflavin, the precursor for the cofactors flavin mononucleotide (FMN) and flavin adenine dinucleotide, is an essential metabolite in all organisms. While the functions for de novo riboflavin biosynthesis and riboflavin import may coexist in bacteria, the extent of this co-occurrence is undetermined. The RibM, RibN, RfuABCD and the energy-coupling factor-RibU bacterial riboflavin transporters have been experimentally characterized. In addition, ImpX, RfnT and RibXY are proposed as riboflavin transporters based on positional clustering with riboflavin biosynthetic pathway (RBP) genes or conservation of the FMN riboswitch regulatory element. Here, we searched for the FMN riboswitch in bacterial genomes to identify genes encoding riboflavin transporters and assessed their distribution among bacteria. Two new putative riboflavin transporters were identified: RibZ in Clostridium and RibV in Mesoplasma florum. Trans-complementation of an Escherichia coli riboflavin auxotroph strain confirmed the riboflavin transport activity of RibZ from Clostridium difficile, RibXY from Chloroflexus aurantiacus, ImpX from Fusobacterium nucleatum and RfnT from Ochrobactrum anthropi. The analysis of the genomic distribution of all known bacterial riboflavin transporters revealed that most occur in species possessing the RBP and that some bacteria may even encode functional riboflavin transporters from two different families. Our results indicate that some species possess ancestral riboflavin transporters, while others possess transporters that appear to have evolved recently. Moreover, our data suggest that unidentified riboflavin transporters also exist. The present study doubles the number of experimentally characterized riboflavin transporters and suggests a specific, non-accessory role for these proteins in riboflavin-prototrophic bacteria.
Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, México.
Ana
A
Gutiérrez-Preciado
Department of Microbiology and Immunology, Sealy Center for Vaccine Development, University of Texas Medical Branch, Galveston, Texas, United States of America; Department of Pathology, Sealy Center for Vaccine Development, University of Texas Medical Branch, Galveston, Texas, United States of America.
Alfredo Gabriel
AG
Torres
Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, México.
Enrique
E
Merino
Fundación Instituto Leloir, IIBBA-CONICET, Buenos Aires, Argentina.
Hernán Ruy
HR
Bonomi
Fundación Instituto Leloir, IIBBA-CONICET, Buenos Aires, Argentina.
Fernando Alberto
FA
Goldbaum
Department of Microbiology and Immunology, Sealy Center for Vaccine Development, University of Texas Medical Branch, Galveston, Texas, United States of America; Centro de Genómica y Bioinformática, Universidad Mayor, Campus Huechuraba, Santiago, Chile.
Víctor Antonio
VA
García-Angulo
D001419:Bacteria / Q000145:classification / Q000235:genetics* / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism*; D053898:Biosynthetic Pathways; D019143:Evolution, Molecular; D005486:Flavin Mononucleotide / Q000378:metabolism; D016680:Genome, Bacterial; D026901:Membrane Transport Proteins / Q000235:genetics* / Q000378:metabolism*; D010802:Phylogeny; D012256:Riboflavin / Q000096:biosynthesis / Q000378:metabolism*; D058928:Riboswitch / Q000235:genetics
D001426:Bacterial Proteins; D026901:Membrane Transport Proteins; D058928:Riboswitch; D005486:Flavin Mononucleotide; D012256:Riboflavin