The Origins of Cooperative Bacterial Communities 2012

Bacteria live in complex multispecies communities. Intimately interacting bacterial cells are ubiquitous on biological and mineral surfaces in all habitats. Molecular and cellular biologists have unraveled some key mechanisms that modulate bacterial interactions, but the ecology and evolution of these associations remain poorly understood. One debate has focused on the relative importance of cooperation among cells in bacterial communities. Some researchers suggest that communication and cooperation, both within and among bacterial species, have produced emergent properties that give such groups a selective advantage. Evolutionary biologists have countered that the appearance of group-level traits should be viewed with caution, as natural selection almost invariably favors selfishness. A recent theory by Morris, Lenski, and Zinser, called the Black Queen Hypothesis, gives a new perspective on this debate (J. J. Morris, R. E. Lenski, and E. R. Zinser, mBio 3(2):e00036-12, 2012). These authors present a model that reshapes a decades-old idea: cooperation among species can be automatic and based upon purely selfish traits. Moreover, this hypothesis stands in contrast to the Red Queen Hypothesis, which states that species are in constant evolutionary conflict. Two assumptions serve as the core of the Black Queen model. First, bacterial functions are often leaky, such that cells unavoidably produce resources that benefit others. Second, the receivers of such by-products will tend to delete their own costly pathways for those products, thus building dependency into the interactions. Although not explicitly required in their model, an emergent prediction is that the initiation of such dependency can favor the spread of more obligate coevolved partnerships. This new paradigm suggests that bacteria might often form interdependent cooperative interactions in communities and moreover that bacterial cooperation should leave a clear genomic signature via complementary loss of shared diffusible functions. Evolutionary adaptation is a special and onerous concept that should not be used unnecessarily, and an effect should not be called a function unless it is clearly produced by design and not by chance. -George C. Williams (7) Much of our understanding of bacteria is from studies of pure cultures. In some cases, single strains of single species have come to represent what scientists know about diverse bacterial lineages. Yet in nature, bacteria almost always exist in complex communities of other species that can be predators or prey, as well as competitors, commensals, mutualists, or pathogens. Despite our appreciation of the ubiquity and importance of bacterial communities, little is known about the cell-cell interactions that form these multispecies consortia. Molecular and cellular biologists have unraveled some of the key mechanisms that modulate bacterial interactions, but there is little understanding of the relative importance of cooperation and conflict in these associations. It is critical to understand the potential for cooperation among bacteria if we are to successfully manage multispecies infections (whether harmful or beneficial to the host) or if we are to engineer bacterial consortia to perform valuable biological tasks. It is also important to discern how and when natural selection can shape cooperation among bacteria. Toward these ends, the opinion piece by Morris, Lenski, and Zinser (1) offers a new perspective on the ecology and evolution of bacterial cooperation. They present a model that reshapes a decades-old idea: that cooperation among individuals can be automatic and based on little more than the production of by-products (e.g., see references 2 and 3). Beyond this core, the model has clear and testable predictions germane to bacterial genomic evolution, the design of novel in vitro methods, and the assembly and stability of bacterial communities. To appreciate the utility of this new model, it is important to introduce a recent controversy over bacterial cooperation. One school of thought is that cooperation among bacteria has produced emergent properties in bacterial communities. Research on two systems, bacterial biofilms and quorum sensing, offers good examples. Biofilms are clonal or multispecies groups of cells defined by their secreted polymers, which help to glue cells together (4). Biofilm communities exhibit several properties that are hypothesized to require molecular communication and cooperation among participating bacteria, including differentiation among cells to produce highly resilient biofilm structures, species stratification to optimize productivity, and the formation of channels to maximize nutrient and oxygen flow (5). In a similar vein, emergent group properties have been highlighted in studies of bacterial quorum sensing, a process in which bacteria secrete and detect diffusible molecular signals to express traits in a contextdependent fashion, usually among members of the same species (4). Detection of released signals in cell groups is thought to allow bacteria to perform functions that would be beneficial only in large populations of cells. Classic examples include the group release of plant-cell-degrading compounds by bacterial phytopathogens and group secretion of virulence compounds in animal pathogens. The idea is that quorum sensing allows the pathogenic traits to be expressed only when the bacterial population numbers are high enough to overwhelm host defenses (4). Thus, both in Published 24 April 2012 Citation Sachs JL, Hollowell AC. 2012. The origins of cooperative bacterial communities. mBio 3(3):e00099-12. doi:10.1128/mBio.00099-12. Copyright © 2012 Sachs and Hollowell. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Address correspondence to J. L. Sachs, joels@ucr.edu. COMMENTARY May/June 2012 Volume 3 Issue 3 e00099-12 ® mbio.asm. org 1 m b.asm . rg on Jauary 9, 2013 P ubished by m b.asm . rg D ow nladed fom biofilms and in quorum sensing, the paradigm has been that evolution has shaped cooperation to maximize the greater good of the group. Yet evolutionary biologists have called ideas of bacterial cooperation into question. The central evolutionary argument is that the relentless action of natural selection favors selfish behavior (6) and that group-level adaptations should be analyzed with care and invoked only when necessary (7). For instance, individual-based models of bacterial movement and attachment can lead to biofilm-like structures in computer simulations, inconsistent with the hypothesis that cell-cell communication is needed to create them (8). Moreover, quorum-sensing traits have also been modeled on the simple terms of individual cell action. Under the “diffusion-sensing” model, single cells selfishly monitor levels of costly diffused products as opposed to coordinating their activities with other cells (9). A difficulty for clarifying predictions for cooperation in bacterial communities has been the lack of predictive models specific to microbe-microbe interactions. The Black Queen Hypothesis by Morris and colleagues (1) makes two basic assumptions about bacterial biology that build a foundation for cooperative community evolution. The first assumption is that some bacterial functions are often leaky. Specifically, bacteria unavoidably produce publicly usable resources, which become available to their local community. This assumption closely mirrors classic models of “by-product mutualism” (2, 3), in which one individual produces a by-product as an automatic effect of its biology and thus enhances the fitness of other individuals that can use that product. By-product mutualism might not seem like a typical form of cooperation, since the “cooperative” phenotype carries no cost and because the trait need not evolve in the context of the interaction. Yet by-products fit well into a broad definition of cooperation: a trait in one individual that increases another’s fitness (10). The second assumption of the model is that a bacterium that uses another’s by-products will benefit from deleting its own costly pathways for those products. Adaptive genome streamlining is known to be common in parasites and symbionts, both of which can benefit from deleting costly functions that are provided by their hosts. When gene loss of vital functions occurs, this builds dependency into the interactions (11). Importantly, these assumptions and the model as a whole can be applied to cooperation within or among bacterial species. Nonetheless, by-product mutualisms based upon resources most often occur among species, since they tend to exhibit divergent resource usage. Morris and colleagues support their assumptions with a diversity of sources. For instance, many empirical studies have shown that bacteria produce by-products that are useful to other cells. Examples of leaky systems include catalase-peroxidase activity (enzymes that break down toxic hydrogen peroxide), production of iron chelators (which make iron soluble for metabolism), and the reduction of sulfur (which is often growth limiting). Such leakiness might be unavoidable because of the nature of diffusion gradients and the need for bacteria to maintain membrane permeability. Morris and colleagues also highlight potential links between by-product utilization and adaptive gene loss. Some very elegant evidence comes from recent studies of the marine bacterium Prochlorococcus. This species is fascinating because it cannot grow in its own natural habitat (sunlit seawater) as a pure culture (12). Prochlorococcus becomes poisoned under these conditions by hydrogen peroxide (which is generated by photooxidation). However, poisoning fails to occur in natural habitats because Prochlo