Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation - PubMed (original) (raw)

Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation

Alexey G Vitreschak et al. Nucleic Acids Res. 2002.

Abstract

The riboflavin biosynthesis in bacteria was analyzed using comparative analysis of genes, operons and regulatory elements. A model for regulation based on formation of alternative RNA structures involving the RFN elements is suggested. In Gram-positive bacteria including actinomycetes, Thermotoga, Thermus and Deinococcus, the riboflavin metabolism and transport genes are predicted to be regulated by transcriptional attenuation, whereas in most Gram-negative bacteria, the riboflavin biosynthesis genes seem to be regulated on the level of translation initiation. Several new candidate riboflavin transporters were identified (impX in Desulfitobacterium halfniense and Fusobacterium nucleatum; pnuX in several actinomycetes, including some Corynebacterium species and Strepto myces coelicolor; rfnT in Rhizobiaceae). Traces of a number of likely horizontal transfer events were found: the complete riboflavin operon with the upstream regulatory element was transferred to Haemophilus influenzae and Actinobacillus pleuropneumoniae from some Gram-positive bacterium; non-regulated riboflavin operon in Pyrococcus furiousus was likely transferred from Thermotoga; and the RFN element was inserted into the riboflavin operon of Pseudomonas aeruginosa from some other Pseudomonas species, where it had regulated the ribH2 gene.

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Figures

Figure 1

Figure 1

The riboflavin biosynthesis pathway in bacteria. Bacillus gene names are underlined.

Figure 2

Figure 2

Multiple alignment of 58 RFN elements from eubacteria. The first column contains the genome abbreviations (see Table 1). The riboflavin operons, single ribH2 genes, single ribB genes and possible riboflavin transporters are marked in blue, red, magenta and green, respectively. The complementary stems of the RNA secondary structure are shown by arrows in the upper line. Base-paired positions are highlighted by the yellow background. Conserved positions and non-consensus nucleotides are shown in red and blue, respectively. Black indicates non-conserved positions. The lengths of additional (Add.) and variable stem–loops are given.

Figure 3

Figure 3

The conserved structure of the RFN element. Upper case letters, invariant (absolutely conserved) positions; lower case letters, strongly conserved positions. Dashes and asterisks indicate obligatory and facultative base pairs, respectively. Degenerate positions: R = A or G; Y = C or U; K = G or U; B = not A; V = not U. N, any nucleotide; X, any nucleotide or deletion.

Figure 4

Figure 4

The predicted mechanism of the _RFN_-mediated regulation of riboflavin genes: (A) transcription attenuation; (B) translation attenuation.

Figure 5

Figure 5

The conserved RNA elements in the upstream regions of the RFN_-regulated genes: (A) the RFN elements and potential terminators; (B) the RFN elements and potential SD-sequestors. The yellow background indicates the first stem of the RFN element. The blue background indicates the proposed teminator/SD-sequestor. Mangenta text indicates the main stem of the anti-terminator or anti-sequestor. Arrows in the upper line show the complementary stems of these RNA secondary structures. The SD-box and the start codon are shown in green and blue, respectively. The pink background indicates additional helices in the loop of the SD-sequestor. The color code of the genome abbreviations in the first column is as in Figure 3. The presence of two terminators in the upstream region of the S.pneumoniae riboflavin operon is marked by an asterisk. The distinct groups of conserved sequestors from γ_- and β_-_proteobacteria are marked.

Figure 6

Figure 6

The maximum likelihood phylogenetic tree of bacterial riboflavin synthases encoded by the ribH gene. The genome abbreviations are listed in Table 1. The separate branch including the ribH2 genes from some α-proteobacteria and Pseudomonas species is shown by bold lines. The ribH genes likely to be horizontally transferred are boxed.

Figure 7

Figure 7

The multiple alignment of the ribH2 upstream regions from P.fluorescens (PU) and P.syringiae (Psy) and the ribE2 upstream region from P.aeruginosa (PA). The highly conserved RFN elements and the predicted SD-sequestors are boxed. The main stems of the predicted anti-sequestors are shown in bold-face. The predicted SD-boxes and start codons of ribH2 and ribE are underlined. The predicted SD-box, start and stop codons of a possible short leader ORF upstream of ribE are set in bold-face and underlined.

Figure 8

Figure 8

The maximum likelihood phylogenetic tree of the RFN elements. The names of the first genes of the _RFN_-regulated operons are given. The genome abbreviations are listed in Table 1.

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