Indole Production Promotes Escherichia coli Mixed-Culture Growth with Pseudomonas aeruginosa by Inhibiting Quorum Signaling

摘要

Indole production by Escherichia coli , discovered in the early 20th century, has been used as a diagnostic marker for distinguishing E. coli from other enteric bacteria. By using transcriptional profiling and competition studies with defined mutants, we show that cyclic AMP (cAMP)-regulated indole formation is a major factor that enables E. coli growth in mixed biofilm and planktonic populations with Pseudomonas aeruginosa . Mutants deficient in cAMP production ( cyaA ) or the cAMP receptor gene ( crp ), as well as indole production ( tnaA ), were not competitive in coculture with P. aeruginosa but could be restored to wild-type competitiveness by supplementation with a physiologically relevant indole concentration. E. coli sdiA mutants, which lacked the receptor for both indole and N -acyl-homoserine lactones (AHLs), showed no change in competitive fitness, suggesting that indole acted directly on P. aeruginosa . An E. coli tnaA mutant strain regained wild-type competiveness if grown with P. aeruginosa AHL synthase ( rhlI and rhlI lasI ) mutants. In contrast to the wild type, P. aeruginosa AHL synthase mutants were unable to degrade indole. Indole produced during mixed-culture growth inhibited pyocyanin production and other AHL-regulated virulence factors in P. aeruginosa . Mixed-culture growth with P. aeruginosa stimulated indole formation in E. coli cpdA , which is unable to regulate cAMP levels, suggesting the potential for mixed-culture gene activation via cAMP. These findings illustrate how indole, an early described feature of E. coli central metabolism, can play a significant role in mixed-culture survival by inhibiting quorum-regulated competition factors in P. aeruginosa .