Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations

• Published in: Proceedings of the Royal Society. B, Biological sciences Vol. 276; no. 1674; pp. 3759 - 3768
• Main Authors: Perlin, Michael H., Clark, Denise R., McKenzie, Courtney, Patel, Himati, Jackson, Nikki, Kormanik, Cecile, Powell, Cayse, Bajorek, Alexander, Myers, David A., Dugatkin, Lee A., Atlas, Ronald M.
• Format: Journal Article
• Language: English
• Published: England The Royal Society 07.11.2009
• Subjects: Ampicillin - pharmacology; Ampicillin Resistance; Anti-Bacterial Agents - pharmacology; Antibiotic Susceptibility; Antibiotics; Bacteria; beta-Lactamases - genetics; beta-Lactamases - metabolism; Enzymes; Escherichia coli; Escherichia coli - drug effects; Escherichia coli - enzymology; Escherichia coli - genetics; Evolution; Flasks; Genetic Engineering; Materials; Plasmids; Salmonella; Salmonella - drug effects; Salmonella enterica; Salmonella enterica serovar Typhimurium; Serovar Typhimurium; Β-Lactamase
• ISSN: 0962-8452; 1471-2954; 1471-2945
• DOI: 10.1098/rspb.2009.0997

Microbial systems have become the preferred testing grounds for experimental work on the evolution of traits that benefit other group members. This work, based on conceptual and theoretical models of frequency-dependent selection within populations, has proven fruitful in terms of understanding the dynamics of group beneficial or 'public goods' traits within species. Here, we expand the scope of microbial work on the evolution of group-beneficial traits to the case of multi-species communities, particularly those that affect human health. We examined whether β-lactamase-producing Escherichia coli could protect ampicillin-sensitive cohorts of other species, particularly species that could cause human disease. Both β-lactamase-secreting E. coli and, surprisingly, those engineered to retain it, allowed for survival of a large number of ampicillin-sensitive cohorts of Salmonella enterica serovar Typhimurium, including both laboratory and clinical isolates. The Salmonella survivors, however, remained sensitive to ampicillin when re-plated onto solid medium and there was no evidence of gene transfer. Salmonella survival did not even require direct physical contact with the resistant E. coli. The observed phenomenon appears to involve increased release of β-lactamase from the E. coli when present with S. enterica. Significantly, these findings imply that resistant E. coli, that are not themselves pathogenic, may be exploited, even when they are normally selfish with respect to other E. coli. Thus, Salmonella can gain protection against antibiotics from E. coli without gene transfer, a phenomenon not previously known. As a consequence, antibiotic-resistant E. coli can play a decisive role in the survival of a species that causes disease and may thereby interfere with successful treatment.