Article

Bacterial Community Morphogenesis Is Intimately Linked to the Intracellular Redox State

Former address: Department of Biology and Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02139.
Journal of bacteriology (Impact Factor: 2.69). 01/2013; 195(7). DOI: 10.1128/JB.02273-12
Source: PubMed

ABSTRACT Many microbial species form multicellular structures, comprising elaborate wrinkles and concentric rings, yet the rules governing their architecture are poorly understood. The opportunistic pathogen Pseudomonas aeruginosa produces phenazines, small molecules that act as alternate electron acceptors to oxygen and nitrate to oxidize the intracellular redox state and that influence biofilm morphogenesis. Here, we show that the depth occupied by cells within colony biofilms correlates well with electron acceptor availability. Perturbations in the environmental provision, endogenous production, and utilization of electron acceptors affect colony development in a manner consistent with redox control. Intracellular NADH levels peak before the induction of colony wrinkling. These results suggest that redox imbalance is a major factor driving the morphogenesis of P. aeruginosa biofilms and that wrinkling itself is an adaptation that maximizes oxygen accessibility and thereby supports metabolic homeostasis. This type of redox-driven morphological change is reminiscent of developmental processes that occur in metazoans.

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Available from: Lars E. Dietrich, May 13, 2014
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    • "It has been reported that the redox status is highly critical for the microorganisms to cope with environmental stresses (Cannon and Remington, 2009; Morgan et al., 2011). The intracellular redox state has been demonstrated to have a great impact in driving the morphological development of biofilms (Dietrich et al., 2013). To understand the role of redox state in biofilm development and responses of biofilms to environmental perturbations, it is essential to quantify the redox state of microenvironments in biofilms. "
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    • "As only shortly mentioned in this review, macrocolony biofilms also exhibit striking macroscopic morphological patterns of ridges, rings and wrinkles, a phenotype that has been termed 'wrinkled', 'rugose' or 'rdar' ('rough, dry and red', with 'redness' depending on the use of the dye Congo Red), although these simple designations do not adequately reflect the complexity and diversity of these structures, which are drastically modulated by oxygen content, the presence of reactive oxygen species or salt or the humidity at the agar surface (Römling, 2005; Aguilar et al., 2007; Beyhan et al., 2007; DePas et al., 2013; Dietrich et al., 2013; Kolodkin-Gal et al., 2013; Serra et al., 2013a). A common signature of these structures is their strict dependence on extracellular matrix components (Friedman and Kolter, 2004; Römling, 2005; Romero et al., 2010; Colvin et al., 2012; Serra et al., 2013a,b), which confer the connectivity and elasticity that allow growing bacterial biofilms to essentially behave as tissues that buckle up under the spatial constraints and therefore tension generated by cellular crowding (Serra et al., 2013a; Trejo et al., 2013). "
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    • "The abundance of phenazines could then offer an alternative electron acceptor in oxygen limited conditions, thereby increasing 2,3-butanedione production and growth or survival of acetoin metabolizing strains (for example, Streptococcus spp.). Phenazine producing mutants of P. aeruginosa have been shown to form biofilms with architecture that increases surface area to increase access to oxygen, supporting the role of phenazines as alternative electron acceptors when access to oxygen is reduced (Dietrich et al., 2013). As shown in Figure 7b, phenazines that accept electrons from NADH that is produced in the course of microbial catabolism may recycle their redox state when they come into contact with O 2 or Fe 3 þ , depending on oxygen availability, pH and the redox potential of the phenazine (Wang and Newman, 2008). "
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