Editorial: Signals to sociality: how microbial communication fashions communities

FEMS Microbiology Reviews, fuw039, 40, 2016, 795–797 doi: 10.1093/femsre/fuw039 Advance Access Publication Date: 27 September 2016 Editorial Editorial: Signals to sociality: how microbial communication fashions communities the utility of quorum sensing for testing evolutionary models about cooperation by reviewing broader questions about microbial social behaviors. The authors consider how a community promotes cooperation amongst its constituents and prevents the emergence and proliferation of cheaters that could disrupt the social order. Asfahl and Schuster dissect the current models for cooperation and persuasively argue for the continued use of bacteria and quorum sensing as a tractable model for examining the evolution of social behaviors. The observation that quorum sensing can control bacterial virulence (Williams et al. 2000) supported investigations into whether disrupting quorum-sensing conversations that lead to sociality could have therapeutic benefits. For example, a quorum-sensing antagonist has been shown to reduce virulence in mice and may prove to be clinically relevant (Starkey et al. 2014). Welsh and Blackwell discuss how such synthetic quorumsensing molecules could also be used to probe for new biological insights into microbial physiology and community structures. Starting from an inclusive view of quorum sensing from a chemical perspective, the authors provide a refreshing evaluation of what other aspects of the biology and physiology of bacteria could be understood through synthetically altering quorum-sensing pathways, or in other words, how changing to a new ‘microbial dialect’ could reveal unknown behaviors. Significantly, the authors also posit that increasing knowledge about metabolic pathways impacted by quorum sensing has the potential to identify new pathways that could be directly targeted in future drug development. In a similar vein, Okada and Seyedsayamodst describe how secondary metabolites produced by one organism can be used to probe secondary metabolism in other organisms and even lead to the discovery of novel antibiotics. In reviewing how antibiotics themselves can be potent inducers of biosynthetic pathways when used at subinhibitory concentrations, the authors posit that these small molecules comprise a previously unappreciated ‘microbial vocabulary’ for mediating intra- and interspecies and interkingdom conversations. They further submit the intriguing hypothesis that if antibiotics are a bonafide form of cell–cell communication, antibiotic resistance ‘may be akin to putting headphones on’ and unplugging from the conversation. The diversity of small molecules produced by bacteria implies that equally diverse processes mediate communication between microbes. These dialogues could be for coordinating populations, as suggested by traditional quorum sensing, managing survival in mixed populations, or navigating changing environmental conditions. Indeed, the majority of bacterial life  C FEMS 2016. All rights reserved. For permissions, please e-mail: 795 The unicellular and liquid-dwelling lifestyles of bacteria have historically dominated microbiological studies, yet most bacteria exist in nature in multifaceted communities that are often associated with living and non-living surfaces. Within these communities, bacteria are exchanging information with other bacteria and other organisms, including eukaryotes, to generate coordinated behaviors. Central to this microbial information exchange is communication between cells. The act of communication exists in many forms and is often considered essential for organized group behaviors between individuals and for the development of multicellular organisms. The collection of reviews presented in the thematic issue ‘Signals to sociality: how microbial communication fashions communities’ (bit.ly/MicrobialCom) addresses several outstanding questions in microbial cell–cell communication. These reviews highlight aspects of cell–cell communication through the lens of microbial linguistics (which signals are communicated and how), microbial ecology and evolution (how communication impacts individuals within communities over time), microbial sociology (‘sociomicrobiology’ (Parsek and Greenberg 2005), how communication impacts group behaviors), and microbial chemistry (what the intrinsic nature of these signaling molecules is). Our knowledge of microbial cell–cell communication is vast and rapidly expanding. Traditional quorum sensing was the first mode of cell–cell communication to be described (Nealson, Platt and Hastings 1970; Engebrecht, Nealson and Silverman 1983; Kaplan and Greenberg 1987; Bassler et al. 1993) and is generally considered to be the control of gene expression in response to cell-population density through the production of and response to freely diffusible small molecules. A large number of organisms produce and respond to more than one quorum-sensing molecule, enabling many ‘conversations’ to be conducted simultaneously. In this issue, Hawver et al. consider the fascinating question of how Vibrio cholerae, and other bacteria, distinguish between the quorum-sensing molecule(s) they produce and those to which they respond and adjust their behavior accordingly, a behavior that is metaphorically analogous to leaning in to hear a conversation amidst the din of a cocktail party. The authors discuss how this listening specificity is rooted in the evolution of quorum-sensing receptors with exquisite specificity for their ligand and broaden this discussion to examine why some microbes have evolved greater complexity in their quorum-sensing pathways. Evolutionary questions about the establishment and maintenance of group behaviors can also be queried with respect to quorum sensing. In this issue, Asfahl and Schuster address 796 FEMS Microbiology Reviews, 2016, Vol. 40, No. 6 that its meaning is translated similarly across distantly related organisms. Similarly, cell–cell communication is present in unicellular eukaryotes. Reid and Latty discuss how eukaryotic microbes can serve as models for cell–cell communication and social behaviors. The authors more broadly consider whether the observed group behaviors of two slime molds (Dictyostelium discoideum and Physarum polycephalum) are examples of ‘collective intelligence’. One definition for collective intelligence is the ability for a group of organisms to perform tasks with greater success and/or efficiency than any given individual within the population as observed for ant colonies (Sumpter 2006), calling to mind Aristotle’s quote that the complete is more than the sum of its pieces. Reid and Latty put forward the provocation that both Physarum and Dictyostelium can be considered models of collective intelligence, following the same guiding principles as for more complex organisms. One is then left considering whether guiding principles developed by studying these eukaryotic microbes could be applied to group behaviors obser (...truncated)