Social interactions in bacterial cell–cell signaling

FEMS Microbiology Reviews, fuw038, 41, 2017, 92–107 doi: 10.1093/femsre/fuw038 Advance Access Publication Date: 2 September 2016 Review Article REVIEW ARTICLE Social interactions in bacterial cell–cell signaling Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, OR 97331-3804, USA ∗ Corresponding author: Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, OR 97331-3804, USA. Tel: +1-541-737-3496; E-mail: One sentence summary: The authors review current research on the evolution and maintenance of microbial communication and cooperation from both a theoretical and experimental perspective. Editor: Karine Gibbs † Kyle L. Asfahl, http://orcid.org/0000-0001-5626-3529 ABSTRACT Cooperation and conflict in microorganisms is being recognized as an important factor in the organization and function of microbial communities. Many of the cooperative behaviors described in bacteria are governed through a cell–cell signaling process generally termed quorum sensing. Communication and cooperation in diverse microorganisms exhibit predictable trends that behave according to social evolutionary theory, notably that public goods dilemmas produce selective pressures for divergence in social phenotypes including cheating. In this review, we relate the general features of quorum sensing and social adaptation in microorganisms to established evolutionary theory. We then describe physiological and molecular mechanisms that have been shown to stabilize cooperation in microbes, thereby preventing a tragedy of the commons. Continued study of the role of communication and cooperation in microbial ecology and evolution is important to clinical treatment of pathogens, as well as to our fundamental understanding of cooperative selection at all levels of life. Keywords: quorum sensing; game theory; microbial cooperation; evolutionary biology; adaptation; evolutionarily stable strategy INTRODUCTION Cooperation among individuals is a common strategy affecting natural selection at every level of life, from genes in genomes (Burt and Trivers 2006) to humans in global societies (Hardin 1968; Kollock 1998). Cooperative interactions typify states of stabilization along an evolutionary progression that has ultimately resulted in the complex and interconnected ecology of life we currently observe (Maynard Smith and Szathmary 1995). With such a fundamental role for cooperation in the underlying ecology of the natural world, understanding the evolutionary origins and maintenance of cooperation has become a primary theme in biological research. While not required for all cooperative interactions, communication among neighboring individuals is often deployed as a mechanism to coordinate cooperative strategies. At the scale of single cells, cooperation among microorganisms has provided a clear window for viewing complex evolutionary phenomena, enabling insights into mechanisms where similar studies of larger organisms have struggled (West et al. 2007). We now understand that many bacteria communicate in a process generally referred to as ‘quorum sensing’ (QS). Originally discovered in Gram-negative Proteobacteria, the diversity of bacterial taxa harboring QS componentry has grown to include hundreds of species across most known bacterial phyla (Manefield and Turner 2002; Case, Labbate and Kjelleberg 2008; Pereira, Thompson and Xavier 2013). QS is now understood to mediate cooperative behaviors as diverse as light production during endosymbiosis with cephalopods (Fuqua, Winans and Greenberg 1994), air vesicle formation that allows vertical migration of planktonic bacteria in aquatic habitats (Ramsay et al. 2011), biofilm formation (Davies et al. 1998) and virulence factor production (Van Delden and Iglewski 1998). Many of these QS-regulated phenotypes exhibit the tell-tale signs of a cooperative ‘public good’ and Received: 19 April 2016; Accepted: 14 August 2016  C FEMS 2016. All rights reserved. For permissions, please e-mail: 92 Kyle L. Asfahl† and Martin Schuster∗ Asfahl and Schuster evolution and maintenance of microbial cooperation in general. We start with a general overview of bacterial QS and cooperative behaviors, followed by theoretical treatments of social evolution. We will then focus on empirical evidence examining the maintenance of cooperative behavior in bacteria and microbes in general. We conclude with applications of social evolutionary research in microbes and highlight some remaining questions and new directions in the field. PRINCIPLES OF BACTERIAL SIGNALING AND SELECTION Microbial growth The general features of microbial growth and selection provide an excellent model system to investigate cooperative and competitive interactions among cells. Bacteria are especially fit for experimentation. Bacteria exhibit the fastest generation times of any independent biological organism, in some cases under 30 min with optimal conditions, permitting the observation of evolutionary change essentially in real time. The ability to easily achieve clonality in routine cultivation is an instrumental advantage. These features, when coupled with the ease of selective pressure manipulation, genetic tractability of model microbial organisms, general ease of handling and relatively large effective population sizes, extend excellent opportunities for experimental evolution studies (Elena and Lenski 2003). Signaling circuitry Bacterial cell–cell signaling was termed QS in 1994 and has been thoroughly characterized over roughly the past 30 years (Fuqua, Winans and Greenberg 1994). QS is widespread in prokaryotes and much of the literature to date has focused on the two most well-understood mechanisms: acyl-homoserine lactone (AHL) signaling in Gram-negative bacteria, and peptide-QS in Grampositive bacteria (Waters and Bassler 2005). With both mechanisms, a small pheromone-like signal is released and received by participating members of a population, allowing surveillance of population density. The molecular architecture and regulatory processes allowing both AHL and peptide-QS signaling have received considerable attention in the literature (Schuster et al. 2013; Cook and Federle 2014), so we are restricting our coverage here to include only the concepts that are necessary to understand their role in social evolution. The common QS componentry in both types of signaling includes a signal synthase, the autoinducer signal and a signal receptor-regulator (Fig. 1). These components were initially characterized in the QS-archetype Vibrio fischeri, yielding a well-studied model of the circuitry (LuxItype AHL synthase and LuxR-type receptor-regulator) that has served as a guide for defining other systems (Eberhard et al. 1981; Engebrecht, Nealson and Silverman 1983; Engebrecht and Silverman 1984). It is important to note that other bacterial QS mechanisms have been described in the literature in addition to AHL- and peptide-based QS. These include hydro (...truncated)