Evaluation of the Role of the opgGHOperon in Yersinia pseudotuberculosisand Its Deletion during the Emergence of Yersinia pestis

ABSTRACTThe opgGHoperon encodes glucosyltransferases that synthesize osmoregulated periplasmic glucans (OPGs) from UDP-glucose, using acyl carrier protein (ACP) as a cofactor. OPGs are required for motility, biofilm formation, and virulence in various bacteria. OpgH also sequesters FtsZ in order to regulate cell size according to nutrient availability. Yersinia pestis(the agent of flea-borne plague) lost the opgGHoperon during its emergence from the enteropathogen Yersinia pseudotuberculosis. When expressed in OPG-negative strains of Escherichia coliand Dickeya dadantii, opgGHfrom Y. pseudotuberculosisrestored OPGs synthesis, motility, and virulence. However, Y. pseudotuberculosisdid not produce OPGs (i) under various growth conditions or (ii) when overexpressing its opgGHoperon, its galUFoperon (governing UDP-glucose), or the opgGHoperon or Acp from E. coli. A ΔopgGHY. pseudotuberculosisstrain showed normal motility, biofilm formation, resistance to polymyxin and macrophages, and virulence but was smaller. Consistently, Y. pestiswas smaller than Y. pseudotuberculosiswhen cultured at ≥37°C, except when the plague bacillus expressed opgGH. Y. pestisexpressing opgGHgrew normally in serum and within macrophages and was fully virulent in mice, suggesting that small cell size was not advantageous in the mammalian host. Lastly, Y. pestisexpressing opgGHwas able to infect Xenopsylla cheopisfleas normally. Our results suggest an evolutionary scenario whereby an ancestral Yersiniastrain lost a factor required for OPG biosynthesis but kept opgGH(to regulate cell size). The opgGHoperon was presumably then lost because OpgH-dependent cell size control became unnecessary.