Microbes are not bound by sociobiology: Response to Kümmerli and Ross‐Gillespie (2013)

Rainey, Paul B.; Desprat, Nicolas; Driscoll, William W.; Zhang, Xuexian

doi:10.1111/evo.12508

Cited by 25 publications

(29 citation statements)

References 56 publications

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“…A particularly pressing issue concerns the ecological significance of adhesive traits in environments where expression of these traits is subject to gene regulation (Gal et al, 2003;Giddens et al, 2007), as opposed to overexpression upon mutational activation, which is the norm in laboratory models of evolution. This requires that the mechanistic insight stemming from use of microbial model systems be applied to natural communities (Rainey et al, 2014), where, despite their often daunting complexity, there exists opportunity to explore the contribution of ecological differences among species to community structure, function and evolution (Jessup et al, 2004).…”

Section: Evolutionary Convergencementioning

confidence: 99%

Evolutionary convergence in experimental Pseudomonas populations

2016

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Model microbial systems provide opportunity to understand the genetic bases of ecological traits, their evolution, regulation and fitness contributions. Experimental populations of Pseudomonas fluorescens rapidly diverge in spatially structured microcosms producing a range of surfacecolonising forms. Despite divergent molecular routes, wrinkly spreader (WS) niche specialist types overproduce a cellulosic polymer allowing mat formation at the air-liquid interface and access to oxygen. Given the range of ways by which cells can form mats, such phenotypic parallelism is unexpected. We deleted the cellulose-encoding genes from the ancestral genotype and asked whether this mutant could converge on an alternate phenotypic solution. Two new traits were discovered. The first involved an exopolysaccharide encoded by pgaABCD that functions as cell-cell glue similar to cellulose. The second involved an activator of an amidase (nlpD) that when defective causes cell chaining. Both types form mats, but were less fit in competition with cellulose-based WS types. Surprisingly, diguanylate cyclases linked to cellulose overexpression underpinned evolution of poly-beta-1,6-N-acetyl-D-glucosamine (PGA)-based mats. This prompted genetic analyses of the relationships between the diguanylate cyclases WspR, AwsR and MwsR, and both cellulose and PGA. Our results suggest that c-di-GMP regulatory networks may have been shaped by evolution to accommodate loss and gain of exopolysaccharide modules facilitating adaptation to new environments.

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Section: Evolutionary Convergencementioning

confidence: 99%

Evolutionary convergence in experimental Pseudomonas populations

2016

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“…Siderophores, by necessity, are secreted, and there has been interest in and debate over the cooperative nature of siderophore production (7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17). In the simplest case, a siderophore, once secreted, is available to all members of a community.…”

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confidence: 99%

Sociality in Escherichia coli: Enterochelin Is a Private Good at Low Cell Density and Can Be Shared at High Cell Density

Scholz

Greenberg

2015

J. Bacteriol.

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Many bacteria produce secreted iron chelators called siderophores, which can be shared among cells with specific siderophore uptake systems regardless of whether the cell produces siderophores. Sharing secreted products allows freeloading, where individuals use resources without bearing the cost of production. Here we show that the Escherichia coli siderophore enterochelin is not evenly shared between producers and nonproducers. Wild-type Escherichia coli grows well in low-iron minimal medium, and an isogenic enterochelin synthesis mutant (⌬entF) grows very poorly. The enterochelin mutant grows well in low-iron medium supplemented with enterochelin. At high cell densities the ⌬entF mutant can compete equally with the wild type in lowiron medium. At low cell densities the ⌬entF mutant cannot compete. Furthermore, the growth rate of the wild type is unaffected by cell density. The wild type grows well in low-iron medium even at very low starting densities. Our experiments support a model where at least some enterochelin remains associated with the cells that produce it, and the cell-associated enterochelin enables iron acquisition even at very low cell density. Enterochelin that is not retained by producing cells at low density is lost to dilution. At high cell densities, cell-free enterochelin can accumulate and be shared by all cells in the group. Partial privatization is a solution to the problem of iron acquisition in low-iron, low-cell-density habitats. Cell-free enterochelin allows for iron scavenging at a distance at higher population densities. Our findings shed light on the conditions under which freeloaders might benefit from enterochelin uptake systems. IMPORTANCESociality in microbes has become a topic of great interest. One facet of sociality is the sharing of secreted products, such as the iron-scavenging siderophores. We present evidence that the Escherichia coli siderophore enterochelin is relatively inexpensive to produce and is partially privatized such that it can be efficiently shared only at high producer cell densities. At low cell densities, cell-free enterochelin is scarce and only enterochelin producers are able to grow in low-iron medium. Because freely shared products can be exploited by freeloaders, this partial privatization may help explain how enterochelin production is stabilized in E. coli and may provide insight into when enterochelin is available for freeloaders. Iron is an essential nutrient for the vast majority of bacteria (1, 2). However, under aerobic conditions at neutral pH, iron is found predominantly in insoluble Fe 3ϩ compounds, resulting in extremely low iron concentrations in water (about 10 Ϫ18 M) (3). Within a host, available iron is also limited, as many host organisms produce iron-binding molecules, which sequester iron away from bacteria (4). Thus, bacteria have evolved a variety of mechanisms to acquire this resource. One mechanism is to secrete molecules, called siderophores, that bind and solubilize extracellular iron. Different bacteria produce differ...

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“…Our argument of noncooperativity in a public goods‐mediated microbial behavior is also relevant beyond predation. For instance, bacterial iron acquisition is mediated by secretion of public siderophores but whether it is actually a cooperative behavior has been debated recently . Computational models of public goods‐mediated behaviors also suggest that such behaviors can be noncooperative in different ecological contexts …”

Section: Discussionmentioning

confidence: 99%

“…It is certainly not straightforward to apply the lessons learned from animal cooperativity to microbial systems. Although a thorough treatment of this subject is beyond our word limit, some excellent reviews and discussions are available …”

Section: A Variety Of Mechanisms Allow the Evolution Of Cooperativitymentioning

confidence: 99%

Is “Wolf‐Pack” Predation by Antimicrobial Bacteria Cooperative? Cell Behaviour and Predatory Mechanisms Indicate Profound Selfishness, Even when Working Alongside Kin

Marshall

Whitworth

2019

BioEssays

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For decades, myxobacteria have been spotlighted as exemplars of social “wolf‐pack” predation, communally secreting antimicrobial substances into the shared public milieu. This behavior has been described as cooperative, becoming more efficient if performed by more cells. However, laboratory evidence for cooperativity is limited and of little relevance to predation in a natural setting. In contrast, there is accumulating evidence for predatory mechanisms promoting “selfish” behavior during predation, which together with conflicting definitions of cooperativity, casts doubt on whether microbial “wolf‐pack” predation really is cooperative. Here, it is hypothesized that public‐goods‐mediated predation is not cooperative, and it is argued that a holistic model of microbial predation is needed, accounting for predator and prey relatedness, social phenotypes, spatial organization, activity/specificity/transport of secreted toxins, and prey resistance mechanisms. Filling such gaps in our knowledge is vital if the evolutionary benefits of potentially costly microbial behaviors mediated by public goods are to be properly understood.

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Microbes are not bound by sociobiology: Response to Kümmerli and Ross‐Gillespie (2013)

Cited by 25 publications

References 56 publications

Evolutionary convergence in experimental Pseudomonas populations

Evolutionary convergence in experimental Pseudomonas populations

Sociality in Escherichia coli: Enterochelin Is a Private Good at Low Cell Density and Can Be Shared at High Cell Density

Is “Wolf‐Pack” Predation by Antimicrobial Bacteria Cooperative? Cell Behaviour and Predatory Mechanisms Indicate Profound Selfishness, Even when Working Alongside Kin

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