Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance

Abstract

Horizontal gene transfer (HGT) plays a major role in the spread of antibiotic resistance. Of particular concern are Acinetobacter baumannii bacteria, which recently emerged as global pathogens, with nosocomial mortality rates reaching 19–54% (Centers for Disease Control and Prevention, 2013; Joly Guillou, 2005; Talbot et al., 2006). Acinetobacter gains antibiotic resistance remarkably rapidly (Antunes et al., 2014; Joly Guillou, 2005), with multi drug-resistance (MDR) rates exceeding 60% (Antunes et al., 2014; Centers for Disease Control and Prevention, 2013). Despite growing concern (Centers for Disease Control and Prevention, 2013; Talbot et al., 2006), the mechanisms underlying this extensive HGT remain poorly understood (Adams et al., 2008; Fournier et al., 2006; Imperi et al., 2011; Ramirez et al., 2010; Wilharm et al., 2013). Here, we show bacterial predation by Acinetobacter baylyi increases cross-species HGT by orders of magnitude, and we observe predator cells functionally acquiring adaptive resistance genes from adjacent prey. We then develop a population-dynamic model quantifying killing and HGT on solid surfaces. We show DNA released via cell lysis is readily available for HGT and may be partially protected from the environment, describe the effects of cell density, and evaluate potential environmental inhibitors. These findings establish a framework for understanding, quantifying, and combating HGT within the microbiome and the emergence of MDR super-bugs.