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A multidrug resistance plasmid contains the molecular switch for type VI secretion in Acinetobacter baumannii

Significance Although the multidrug-resistant (MDR) bacterium Acinetobacter baumannii is a serious threat for health care systems worldwide, very little is known about the mechanisms that have facilitated its rise as a successful pathogen. Our work demonstrates that multiple MDR A. baumannii strains regulate the expression of their type VI secretion system (T6SS), an antibacterial apparatus used to kill other bacteria, by harboring a large, self-transmissible resistance plasmid containing T6SS regulatory genes. Through spontaneous plasmid loss, A. baumannii activates its T6SS and is able to outcompete other bacteria. However, this comes at a cost, as these strains lose resistance to antibiotics. This mechanism constitutes an apparent survival strategy by A. baumannii and provides insights into the pathobiology of this important pathogen. Infections with Acinetobacter baumannii, one of the most troublesome and least studied multidrug-resistant superbugs, are increasing at alarming rates. A. baumannii encodes a type VI secretion system (T6SS), an antibacterial apparatus of Gram-negative bacteria used to kill competitors. Expression of the T6SS varies among different strains of A. baumannii, for which the regulatory mechanisms are unknown. Here, we show that several multidrug-resistant strains of A. baumannii harbor a large, self-transmissible resistance plasmid that carries the negative regulators for T6SS. T6SS activity is silenced in plasmid-containing, antibiotic-resistant cells, while part of the population undergoes frequent plasmid loss and activation of the T6SS. This activation results in T6SS-mediated killing of competing bacteria but renders A. baumannii susceptible to antibiotics. Our data show that a plasmid that has evolved to harbor antibiotic resistance genes plays a role in the differentiation of cells specialized in the elimination of competing bacteria.