Spatial structure, cooperation and competition in biofilms

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Abstract

Bacteria often live within matrix-embedded communities, termed biofilms, which are now understood to be a major mode of microbial life. The study of biofilms has revealed their vast complexity both in terms of resident species composition and phenotypic diversity. Despite this complexity, theoretical and experimental work in the past decade has identified common principles for understanding microbial biofilms. In this Review, we discuss how the spatial arrangement of genotypes within a community influences the cooperative and competitive cell-cell interactions that define biofilm form and function. Furthermore, we argue that a perspective rooted in ecology and evolution is fundamental to progress in microbiology.

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Microbial biofilms.

J Costerton, Z Lewandowski, D E Caldwell … (1995)

Direct observations have clearly shown that biofilm bacteria predominate, numerically and metabolically, in virtually all nutrient-sufficient ecosystems. Therefore, these sessile organisms predominate in most of the environmental, industrial, and medical problems and processes of interest to microbiologists. If biofilm bacteria were simply planktonic cells that had adhered to a surface, this revelation would be unimportant, but they are demonstrably and profoundly different. We first noted that biofilm cells are at least 500 times more resistant to antibacterial agents. Now we have discovered that adhesion triggers the expression of a sigma factor that derepresses a large number of genes so that biofilm cells are clearly phenotypically distinct from their planktonic counterparts. Each biofilm bacterium lives in a customized microniche in a complex microbial community that has primitive homeostasis, a primitive circulatory system, and metabolic cooperativity, and each of these sessile cells reacts to its special environment so that it differs fundamentally from a planktonic cell of the same species.

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Bacterial quorum-sensing network architectures.

Wai-Leung Ng, Bonnie Bassler (2009)

Quorum sensing is a cell-cell communication process in which bacteria use the production and detection of extracellular chemicals called autoinducers to monitor cell population density. Quorum sensing allows bacteria to synchronize the gene expression of the group, and thus act in unison. Here, we review the mechanisms involved in quorum sensing with a focus on the Vibrio harveyi and Vibrio cholerae quorum-sensing systems. We discuss the differences between these two quorum-sensing systems and the differences between them and other paradigmatic bacterial signal transduction systems. We argue that the Vibrio quorum-sensing systems are optimally designed to precisely translate extracellular autoinducer information into internal changes in gene expression. We describe how studies of the V. harveyi and V. cholerae quorum-sensing systems have revealed some of the fundamental mechanisms underpinning the evolution of collective behaviors.

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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

J Morris, Richard Lenski, Erik R. Zinser (2012)

ABSTRACT Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and “Candidatus Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.