Structural evidence for the evolutionary divergence of mycoplasma from gram-positive bacteria: the histidine-containing phosphocarrier protein

Structure. 1995 Aug 15;3(8):781-90. doi: 10.1016/s0969-2126(01)00213-1.

Abstract

Background: The three-dimensional structures of histidine-containing phosphocarrier protein (HPr), a member of the phosphoenolpyruvate:sugar phosphotransferase system (PTS), have been determined from Gram-negative and Gram-positive bacteria. The structure of HPr reported here for Mycoplasma capricolum is the first protein structure to be determined for this class of organism. Comparative structural studies with the bacterial proteins highlight sequence-structure correlations relevant to proposals about the evolutionary origin of mycoplasmas.

Results: The crystal structure of HPr from M. capricolum has been determined and refined at 1.8 A resolution, revealing the same overall fold as that of other HPrs of known structure. However, mycoplasma HPr resembles HPrs from Gram-positive bacteria more closely than those from Gram-negative bacteria. As in HPrs from Bacillus subtilis and Escherichia coli, the phosphoryl group carrier (His15) forms the N-terminal cap of a helix, but in contrast to the other crystal structures, the side chain of the adjacent Arg17 is conformationally disordered. A sulfate ion interacts with Ser46, a residue known to be phosphorylated in a regulatory manner.

Conclusions: The greater degree of structural similarity of the M. capricolum HPr to HPrs from Gram-positive rather than Gram-negative bacteria is consistent with the proposal that mycoplasma evolved from Gram-positive bacteria. The proposal that no major conformational transition is required for phosphorylation of the active-site histidine is reinforced by comparing the crystal structures with and without an anion in the active site. The conformational disorder of the Arg17 side chain suggests that its guanidinium group does not have to form specific interactions with other protein groups before phosphorylation at His15. The association of a sulfate ion with Ser46 serves as a model for HPr(Ser46-P). As there is no evidence of a conformational change accompanying Ser46 phosphorylation, the inhibitory effect of this event may be attributable to altered surface electrostatics.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Bacillus subtilis / genetics
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Biological Evolution*
  • Crystallography, X-Ray
  • Enterococcus faecalis / genetics
  • Escherichia coli / genetics
  • Fourier Analysis
  • Gram-Positive Bacteria / genetics*
  • Models, Molecular
  • Molecular Sequence Data
  • Mycoplasma / genetics*
  • Phosphoenolpyruvate Sugar Phosphotransferase System / chemistry*
  • Phosphoenolpyruvate Sugar Phosphotransferase System / genetics*
  • Phosphoenolpyruvate Sugar Phosphotransferase System / isolation & purification
  • Protein Structure, Secondary*
  • Sequence Homology, Amino Acid

Substances

  • Bacterial Proteins
  • Phosphoenolpyruvate Sugar Phosphotransferase System
  • phosphocarrier protein HPr