Flagellar export apparatus and ATP synthetase: Homology evidenced by synteny predating the Last Universal Common Ancestor

Abstract

We report evidence further supporting homology between proteins in the F1FO‐ATP synthetase and the bacterial flagellar motor (BFM). BFM proteins FliH, FliI, and FliJ have been hypothesized to be homologous to FO‐b + F1‐δ, F1‐α/β, and F1‐γ, with similar structure and interactions. We conduct a further test by constructing a gene order dataset, examining the order of fliH, fliI, and fliJ genes across the phylogenetic breadth of flagellar and nonflagellar type 3 secretion systems, and comparing this to published surveys of gene order in the F1FO‐ATP synthetase, its N‐ATPase relatives, and the bacterial/archaeal V‐ and A‐type ATPases. Strikingly, the fliHIJ gene order was deeply conserved, with the few exceptions appearing derived, and exactly matching the widely conserved F‐ATPase gene order atpFHAG, coding for subunits b‐δ‐α‐γ. The V/A‐type ATPases have a similar conserved gene order. Our results confirm homology between these systems, and suggest a rare case of synteny conserved over billions of years, predating the Last Universal Common Ancestor (LUCA).

The rapid evolution of flagellar ion selectivity in experimental populations of E. coli

“…The flagellar system and its regulatory elements have been known to be under selective pressure due to their associated energetic and fitness costs, not only always resulting in positive selection but also often resulting in gene deletion or inactivation by insertion sequences (29)(30)(31)(32)(33)(34). By targeting the stator subunit of the flagellar motor, we have been able to study the molecular events leading to the spontaneous adaptation of a unique module within a highly conserved molecular complex (35).…”

Questioning physiological rotary functionality in the bacterial flagellar system and proposing a murburn model for motility

“…Examples of such jet-propulsion type logic are known in the microbial world and the physics-math of this theory is also justified (Spagnolie & Lauga, 2010). The role of Complex V has been shown to be one of ATP-based pore, which is quite analogous to the basal module function proposed here; and which is supported by the fact that the basal module of BFS, by virtue of being a T3SS, has a Complex V-type of structure at the base of the flagellar filament (Matzke et al, 2021). Further, this is the logic of some man-made nanomotors (Kim et al,2016)!…”

“…The murburn model does not solicit or necessitate adherence to relative stoichiometries in the C-ring or Mot or MSLP proteins. The BFS proteins FliH, FliI, and FliJ are homologous to F O -b + F 1 -δ, F 1 -α/β, and F 1 -γ (respectively) and the fliHIJ gene order was deeply conserved and found matching the widely conserved F-ATPase gene order atpFHAG, coding for subunits b-δ-α-γ (Matzke et al, 2021).…”

“…Under this purview, the BFS assembly of multiple rings (M, S, L, P) can be seen as an efficient way to maintain a tight fit of the flagellum with the cell membrane/wall. Reports of the known ATPase activity of the basal module and its analogy with Complex V is well explored now (Albertini et al, 1991;Vogler et al, 1991;Matzke et al, 2021). Table 1 presents a comparison of the earlier and current models.…”

The rapid evolution of flagellar ion-selectivity in experimental populations ofE. coli

“…The flagellar system and its regulatory elements have been known to be under selective pressure due to their associated energetic and fitness costs, not always resulting in positive selection but also often resulting in gene deletion or inactivation by insertion sequences (28)(29)(30)(31)(32)(33). By targeting the stator subunit of the flagellar motor, we have been able to study the molecular events leading to the spontaneous adaptation of a unique module within a highly conserved molecular complex (34).…”