Morgan N. Price
The bacterial flagellum, which allows many bacteria to swim, is enabled by about two dozen conserved proteins that form its structure and/or aid in its assembly. Flagellar genes from several phyla of bacteria are found in giant operons with consistent gene order, albeit with various insertions of other flagellar genes. Thus, the ancestral bacterial flagellum was probably encoded by a giant operon that contained the sequence fliEFGHILMNOPQR-flhBA. The type III secretion systems, which are distant relatives of the flagellum, also have the gene order fliMPQR-flhBA.
A recent analysis proposed that the ancestor of Bacteria had small, usually two-gene flagellar operons, and that there was an evolutionary trend towards increasing cluster size (Liu and Ochman 2007). However, this analysis only considered operons that are present in the well-studied bacterium Escherichia coli. Flagellar genes are often clustered together, and I suspected that these huge clusters contained large operons, but with a different ordering or combination of genes than in E. coli, so that the operons were not recognized in the previous analysis.
As a preliminary test of this hypothesis, I searched for experimental data on the operon structures for flagellar genes across the bacteria. I found experimental evidence for large operons in several lineages, as listed in the table below. Within each operon, "*" indicates that adjacent genes are in the same operon in this organism, but are in different operons in E. coli. Genes that are not core flagellar genes (as defined by Liu and Ochman 2007) are in parentheses. In B. subtilis and E. coli, "|" indicates internal promoters.
|Organism||Phylogenetic Group||Operon structures||References|
|*fliA(ylxL) 1 operon, 3 internal promoters
|Estacio98, West00, deHoon05|
*fliL*fliM*fliNOPQR*flhBA(flhF-flbE) 1 operon
|Caulobacter crescentus||alpha-Proteobacteria ("group I")||
(fliO)fliP 4 operons
|Rhodobacter sphaeroides||alpha-Proteobacteria ("group II")||
|Sinorhizobium meliloti||alpha-Proteobacteria ("group II")||
|Vibrio parahaemolyticus||gamma-Proteobacteria (non-enteric "main" polar flagellum)||
|Escherichia coli||gamma-Proteobacteria (enteric)||
Caveat: In S. meliloti, direct evidence for co-transcription is lacking. However, the regulation of these genes has been studied, and some promoters have been identified. The huge size of this gene cluster (51 genes), which is largely conserved in other alpha-Proteobacteria (e.g., Agrobacterium tumefaciens), also suggests that large operons are present.
The B. subtilis and B. burgerdorferi giant operons contain 18 genes in common that are in the same order. 13 of those genes are in the same order and co-transcribed in the gamma-Proteobacterium Vibrio parahaemolyticus as well (fliE*FGHI*..L..MNOPQR*flhB). Although these 13 genes seem to be spread across 4 operons in E. coli, they are all adjacent except for flhB.
Furthermore, a similar gene order fliMPQR-flhBA is found in putative Type III secretion systems. For example, Myxococcus xanthus DK 1622, beginning with MXAN_5649, contains the genes fliM-?-escR-fliQ-escT-flhB-escV. (The gene names are from their COG assignments, see here.) escR is a distant homolog of fliP, and similarly escT=fliR, escV=flhA (and fliM is also known as hrcQ, and flhBis known as hrpN).
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