Modularity of stress response evolution

Singh, Amoolya H.; Wolf, Denise M.; Wang, Peggy; Arkin, Adam P.

doi:10.1073/pnas.0709764105

Cited by 54 publications

(38 citation statements)

References 44 publications

(46 reference statements)

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“…Phylogenetic data are also consistent with our conjecture for an evolutionary progression from motility to chemotaxis. Whereas the flagellar genes are highly conserved among motile species, the sensing, signal transduction, and transcription factors associated with chemotaxis vary among species and habitats and are used with modifications for diverse cellular tasks (35)(36)(37)(38)(39)(40).…”

Section: Discussionmentioning

confidence: 99%

The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility

Wei

Wang

Liu

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Why is motility so common in bacteria? An obvious answer to this ecological and evolutionary question is that in almost all habitats, bacteria need to go someplace and particularly in the direction of food. Although the machinery required for motility and chemotaxis (acquiring and processing the information needed to direct movement toward nutrients) are functionally coupled in contemporary bacteria, they are coded for by different sets of genes. Moreover, information that resources are more abundant elsewhere in a habitat would be of no value to a bacterium unless it already had the means to get there. Thus, motility must have evolved before chemotaxis, and bacteria with flagella and other machinery for propulsion in random directions must have an advantage over bacteria relegated to moving at the whim of external forces alone. However, what are the selection pressures responsible for the evolution and maintenance of undirected motility in bacteria? Here we use a combination of mathematical modeling and experiments with Escherichia coli to generate and test a parsimonious and ecologically general hypothesis for the existence of undirected motility in bacteria: it enables bacteria to move away from each other and thereby obtain greater individual shares of resources in physically structured environments. The results of our experiments not only support this hypothesis, but are quantitatively and qualitatively consistent with the predictions of our model. experimental evolution | population dynamics | partial differential equations I f we accept that the presence of genes coding for flagella indicates the phenotype of self-propulsion, motility is an ancient and almost ubiquitous character in the eubacteria. Flagellar genes are significantly overrepresented in environmental samples of DNA (1, 2), and almost two-thirds of sequenced bacteria with phenotypic annotations are motile (3). Why is motility so widespread? At a qualitative level the obvious answer is almost certainly true: In most of the habitats in which bacteria reside, nutrients are not evenly dispersed. Cells with the facility to propel themselves have more access to resources than those that move solely at the whim of external forces. This qualitative answer, however, raises a number of quantitative questions that have to be addressed for a comprehensive understanding of the ecological conditions under which natural selection will favor the evolution and maintenance of motility. Under what conditions will the relatively weak propulsion ability of a bacterium enable it to overcome the viscosity (resistance to flow or gumminess) of its environment for its movement to be effective? Under what conditions will movement in random directions provide a bacterium with an edge in the acquisition of resources when competing with bacteria that are nonmotile or less motile? In contemporary bacteria, motility is commonly coupled with chemotaxis, i.e., the sensory and signaling machinery needed to direct their motion toward nutrients (4-6). Logic, retrospective eviden...

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Section: Discussionmentioning

confidence: 99%

The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility

Wei

Wang

Liu

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Note that (i) dates reported for each sequence are publication dates, even if the genome was released to the public earlier in database form, and (ii) the numbers for 2008 represent the available data until June 2008. (57). In the interest of clarity, for Fig.…”

Section: Methodsmentioning

confidence: 99%

Discovering Functional Novelty in Metagenomes: Examples from Light-Mediated Processes

et al. 2009

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The emerging coverage of diverse habitats by metagenomic shotgun data opens new avenues of discovering functional novelty using computational tools. Here, we apply three different concepts for predicting novel functions within light-mediated microbial pathways in five diverse environments. Using phylogenetic approaches, we discovered two novel deep-branching subfamilies of photolyases (involved in light-mediated repair) distributed abundantly in high-UV environments. Using neighborhood approaches, we were able to assign seven novel functional partners in luciferase synthesis, nitrogen metabolism, and quorum sensing to BLUF domain-containing proteins (involved in light sensing). Finally, by domain analysis, for RcaE proteins (involved in chromatic adaptation), we predict 16 novel domain architectures that indicate novel functionalities in habitats with little or no light. Quantification of protein abundance in the various environments supports our findings that bacteria utilize light for sensing, repair, and adaptation far more widely than previously thought. While the discoveries illustrate the opportunities in function discovery, we also discuss the immense conceptual and practical challenges that come along with this new type of data.One of the central questions in biology, starting from the time of Charles Darwin, has been the extent and distribution of biological diversity (68). The recent sequencing of several hundred bacterial and archaeal genomes and metagenomes, along with the discovery of large-scale lateral gene transfer (10) and recombination (25) in bacterial evolution, has not only renewed interest in the question of diversity but also confounded it. The sequencing projects reveal that contrary to previous estimates, it is microbes that account for the vast majority of diversity in phenotype and genotype on earth (44, 47). Underlying this dazzling diversity in species and habitat is molecular diversity. Indeed, we are just beginning to scratch the surface of this molecular diversity (50). Even though our understanding of how the living world functions at the molecular level is far from complete, the discovery of novel molecules has important applications to medicine, agriculture, industry, and environmental conservation and remediation.But how are we to discover functional novelty in the exponentially increasing amounts of sequenced genes and habitats (Fig.

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“…Recent analyses of stress-regulatory network structure indicate that most of the variation in environmentally responsive gene networks (in both gene sequence and gene content) lies in the sensing and signal-transduction genes that operate at the onset of stress (Singh et al 2008). Phosphorylation events that alter the functional properties of existing cellular proteins are integral to stress sensing and signal transduction.…”

Section: Species Of Mussels Introductionmentioning

confidence: 99%

“…However, the ability to actively regulate effector-protein expression during environmental stress is ultimately dependent on upstream environmental stress sensors and signal transducers, which relay molecular messages to specific effector molecules. As a result, adaptive responses are contingent on the systematic actions of sensors, signal transducers, and effectors (Fiol and Kültz 2007;Evans andSomero 2008, 2009), and they have evolved into complex, multicomponent regulatory networks (Hartwell et al 1999;Feder 2007;Singh et al 2008). However, the appearance of different ecological lifestyles, even among closely related species such as Mytilus congeners in the northeastern Pacific, suggest that despite this inherent complexity, the networks underlying stress adaptation have remained evolvable and capable of responding to different selection pressures associated with specific ecological niches (Singh et al 2008).…”

Section: Species Of Mussels Introductionmentioning

confidence: 99%

Phosphorylation Events Catalyzed by Major Cell Signaling Proteins Differ in Response to Thermal and Osmotic Stress among Native (Mytilus californianusandMytilus trossulus) and Invasive (Mytilus galloprovincialis) Species of Mussels

Evans

Somero²

2010

Physiological and Biochemical Zoology

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Sharp environmental gradients encountered within the intertidal zone have driven the evolution of physiological adaptations that allow its inhabitants to maintain cellular function in the presence of fluctuating abiotic factors. These adaptations are mediated by gene-regulatory networks that, despite their inherent complexity, must remain evolvable and capable of responding to different selection pressures associated with specific ecological niches. Phosphorylation events catalyzed by cell-signaling enzymes represent a parsimonious mechanism to integrate new functional or regulatory properties into these gene-regulatory networks. In this study, proteins phosphorylated on consensus sequences for protein kinases A, B, and C; cyclin-dependent kinases; and mitogen-activated protein kinases, as well as the abundance of phosphorylated stress-activated protein kinase (phospho-SAPK/JNK), were quantified in order to ascertain whether phosphorylation events are divergent among native (Mytilus californianus and Mytilus trossulus) and invasive (Mytilus galloprovincialis) species of mussels that differ in their tolerance toward environmental stress. Abundances of phosphorylated substrate proteins for each of the major signaling proteins that were investigated, as well as the abundance of phospho-SAPK/JNK, differed both within and between species during thermal and osmotic stress. These data suggest that modulating protein function via phosphorylation may be an important mechanism to integrate novel properties into stress-regulatory networks. In turn, differential phosphorylation during environmental stress may contribute to species-specific tolerances toward abiotic stress, interspecies dynamics, and biogeographic patterns in Mytilus congeners.

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Modularity of stress response evolution

Cited by 54 publications

References 44 publications

The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility

The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility

Discovering Functional Novelty in Metagenomes: Examples from Light-Mediated Processes

Phosphorylation Events Catalyzed by Major Cell Signaling Proteins Differ in Response to Thermal and Osmotic Stress among Native (Mytilus californianusandMytilus trossulus) and Invasive (Mytilus galloprovincialis) Species of Mussels

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