Transcription factor levels enable metabolic diversification of single cells of environmental bacteria

Abstract

Transcriptional noise is a necessary consequence of the molecular events that drive gene expression in prokaryotes. However, some environmental microorganisms that inhabit polluted sites, for example, the m-xylene degrading soil bacterium Pseudomonas putida mt-2 seem to have co-opted evolutionarily such a noise for deploying a metabolic diversification strategy that allows a cautious exploration of new chemical landscapes. We have examined this phenomenon under the light of deterministic and stochastic models for activation of the main promoter of the master m-xylene responsive promoter of the system (Pu) by its cognate transcriptional factor (XylR). These analyses consider the role of co-factors for Pu activation and determinants of xylR mRNA translation. The model traces the onset and eventual disappearance of the bimodal distribution of Pu activity along time to the growth-phase dependent abundance of XylR itself, that is, very low in exponentially growing cells and high in stationary. This tenet was validated by examining the behaviour of a Pu-GFP fusion in a P. putida strain in which xylR expression was engineered under the control of an IPTG-inducible system. This work shows how a relatively simple regulatory scenario (for example, growth-phase dependent expression of a limiting transcription factor) originates a regime of phenotypic diversity likely to be advantageous in competitive environmental settings.

Substrate and electron donor limitation induce phenotypic heterogeneity in different metabolic activities in a green sulphur bacterium

“…In combination with the NH 1 4 limitation experiment, the results demonstrate that phenotypic heterogeneity in a certain metabolic activity (i.e., N 2 fixation) can be driven by different modes of limitation (here limitation in NH 1 4 and H 2 S) in a single microbial population (i.e., C. phaeobacteroides). These results might be best understood in terms of a general feedback between growth state and gene expression (Klumpp et al, 2009;Scott et al, 2010;Kiviet et al, 2014;New et al, 2014;Solopova et al, 2014;Kotte et al, 2014;Guantes et al, 2016;Nordholt et al, 2017).…”

“…Phenotypic heterogeneity helps microbial populations (Ackermann, ) to adapt to fluctuating environmental conditions (Balaban et al ., ; Kussell and Leibler, ; Acar et al ., ; Beaumont et al ., ; Ratcliff and Denison, ; Arnoldini et al ., ; Schreiber et al ., ), aids in the division of labour within isogenic cell populations (Ackermann et al ., ) and can result from negative frequency‐dependent interactions in mixed resource environments (Healey et al ., ). Multiple studies on phenotypic heterogeneity have been conducted with microbial model strains, while only a few studies have investigated environmental isolates (Ziv et al ., ; Holland et al ., ; New et al ., ; Miot et al ., ; Guantes et al ., ) or natural microbial populations (Kopf et al ., ; Zimmermann et al ., ; Sheik et al ., ). Thus, there remains a knowledge gap as to how phenotypic heterogeneity is controlled in environmental bacteria without long laboratory culture history and in natural microbial populations.…”

Spatially Correlated Gene Expression in Bacterial Groups: The Role of Lineage History, Spatial Gradients, and Cell-Cell Interactions

“…neighbors having different phenotypes) can facilitate division of labor between cells. This can be of benefit in the context of anabolic pathways: cells can benefit from economies of scale by specializing on the biosynthesis of a subset of metabolites, while exchanging end products with neighbors specializing on complementary pathways (Johnson et al , 2012; Guantes et al , 2015).…”

The emergence of metabolic heterogeneity and diverse growth responses in isogenic bacterial cells

“…Previous studies characterized how genetic composition in a population changes slowly through mutations and becomes diverse in environments where nutrients are limited and fluctuate [4][5][6][7][8][9][10][11]. In recent years, it became clear that a genetically identical population can also diversify phenotypically [12][13][14][15][16][17][18][19][20][21][22][23]. Phenotypic diversity can have significant effects on ecological dynamics of populations and species [24]; for example, it has a critical role in population survival through catastrophic environmental changes [25], promoting sustenance of microbial species [26,27].…”