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Pseudomonad Reverse Carbon Catabolite Repression, Interspecies Metabolite Exchange, and Consortial Division of Labor

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Pseudomonad Reverse Carbon Catabolite Repression, Interspecies Metabolite Exchange, and Consortial Division of Labor Cellular and Molecular Life Sciences (2020) 77:395–413 https://doi.org/10.1007/s00018-019-03377-x Cellular andMolecular Life Sciences REVIEW Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor Heejoon Park1,3 · S. Lee McGill2,3 · Adrienne D. Arnold2,3 · Ross P. Carlson1,2,3 Received: 4 November 2019 / Revised: 4 November 2019 / Accepted: 12 November 2019 / Published online: 25 November 2019 © Springer Nature Switzerland AG 2019 Abstract Microorganisms acquire energy and nutrients from dynamic environments, where substrates vary in both type and abundance. The regulatory system responsible for prioritizing preferred substrates is known as carbon catabolite repression (CCR). Two broad classes of CCR have been documented in the literature. The best described CCR strategy, referred to here as classic CCR (cCCR), has been experimentally and theoretically studied using model organisms such as Escherichia coli. cCCR phenotypes are often used to generalize universal strategies for ftness, sometimes incorrectly. For instance, extremely competitive microorganisms, such as Pseudomonads, which arguably have broader global distributions than E. coli, have achieved their success using metabolic strategies that are nearly opposite of cCCR. These organisms utilize a CCR strategy termed ‘reverse CCR’ (rCCR), because the order of preferred substrates is nearly reverse that of cCCR. rCCR phenotypes prefer organic acids over glucose, may or may not select preferred substrates to optimize growth rates, and do not allocate intracellular resources in a manner that produces an overfow metabolism. cCCR and rCCR have traditionally been interpreted from the perspective of monocultures, even though most microorganisms live in consortia. Here, we review the basic tenets of the two CCR strategies and consider these phenotypes from the perspective of resource acquisition in consortia, a scenario that surely infuenced the evolution of cCCR and rCCR. For instance, cCCR and rCCR metabolism are near mirror images of each other; when considered from a consortium basis, the complementary properties of the two strategies can mitigate direct competition for energy and nutrients and instead establish cooperative division of labor. Keywords Diauxie · Carbon catabolic repression · Reverse carbon catabolic repression · Division of labor · Overfow metabolism Introduction must dynamically change their phenotypes with environ- mental fuctuations to maintain ftness [3]. Metabolic regula- Most natural environments are physically, chemically, and tion of substrate-consumption order is paramount to ftness. temporally complex, with the resident microorganisms There are a few broad strategies that can be utilized when exposed to multifactorial selection pressures. It is not pos- an organism is presented with two potential substrates: (1) sible to optimize all cellular functions simultaneously due to utilize the ‘optimal’ substrate, (2) utilize the less ‘optimal’ constraints on cellular resources such as anabolic nitrogen or substrate, or (3) co-catabolize both substrates simultane- cytoplasmic volume; a concept illustrated by the ‘Darwinian ously (see Box 1 for discussion of ‘optimal’ substrates). It Demon’ thought exercise [1, 2]. Therefore, microorganisms can be more resource efective to catabolize a single sub- strate at a time as opposed to expressing multiple catabolic * Ross P. Carlson pathways simultaneously [4, 5]; although, exceptions exist [email protected] [6]. Carbon catabolite repression (CCR) is a global regula- tion system that controls the sequential catabolism of pre- 1 Department of Chemical and Biological Engineering, ferred substrates from a milieu (Box 2). CCR is associated Montana State University, Bozeman, USA with generalist microorganisms that can utilize multiple 2 Department of Microbiology and Immunology, Montana substrates and exist in environments, where these substrates State University, Bozeman, USA are often available at varying abundances 3 Center for Bioflm Engineering, Montana State University, Bozeman, USA Vol.:(0123456789)1 3 396 H. Park et al. The cCCR regulation scheme, known under specifc con- followed by a lag phase, then a second exponential growth ditions as diauxie, has been the focus of much experimen- phase on the other sugar. Diauxic growth is a trade-of tal and theoretical research [7–12]. The historical basis of between specializing for a single nutrient and being able to cCCR goes back more than 70 years to Jacques Monod and switch between nutrients as conditions change [14]. Com- his observations of Escherichia coli growing in the presence mitting to one metabolism at a time, necessitates a metabolic of glucose and other sugars [13]. Monod recorded E. coli shift when the preferred substrate is exhausted, with a result- cultures growing exponentially on glucose until depleted, ing temporal delay. 1 3 Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and… 397 . by the CCR systems such as quorum sensing, bioflm for- The traditional interpretation of diauxie as being carried mation, and antibiotic or reactive oxygen species (ROS) out by a single population of organisms, synchronized in tolerance have been studied from the perspective of medi- function, that sequentially catabolizes preferred and non- cal challenges and monocultures, even though these behav- preferred substrates has been challenged [15, 16]. Recent iors modulate inter-microbial interactions and strategies for research has posited an alternative interpretation; rather than resource acquisition in consortia (see sections below). a homogenous population, the observed lag phase can be This review summarizes (1) cCCR and rCCR molecular explained by dynamic shifts in subpopulations possessing mechanisms; (2) theory used to interpret and model CCR diferent ftness. For instance, during growth on glucose, phenotypes; and (3) the nexus of CCR, metabolism, and multiple subpopulations catabolize, the sugar but upon glu- cellular interactions. Collectively, the properties of cCCR cose depletion only some subpopulations, in an ecological and rCCR phenotypes can enhance growth and persistence bet-hedging strategy, are phenotypically prepared to con- by enabling cooperation via division of labor, as observed sume the less desirable substrate [17]. The lag in growth in some medical environments such as chronic wounds, between the two sugars corresponds to a shift in subpopula- where cCCR and rCCR microorganisms commonly cooc- tion distributions as ft subpopulations outgrow other sub- cur (Fig. 1). populations [17]. Control of these subpopulations has been associated with the regulation of bistable genetic switches [18, 19]. Molecular mechanisms of CCR cCCR is not used by all glucose-utilizing microorgan- isms. Pseudomonads and Acinetobacter [20] utilize sub- Most CCR studies have been performed in model organisms strates in an order almost reverse of cCCR. Therefore, this such as E. coli and Bacillus subtilis, which prefer glucose metabolic regulatory strategy was termed reverse carbon over other substrates. The regulatory outcomes of CCR in E. catabolite repression (rCCR) or sometimes reverse diauxie. coli and B. subtilis are similar, though the mechanisms dif- rCCR utilizing microorganisms are very competitive as evi- fer (Fig. 2). This review summarizes molecular mechanisms denced by their broad global distributions and are arguably of CCR for context and to highlight similarities and difer- at least as competitive as the better studied members of the ences between cCCR and rCCR (Table 1). This summary is Enterobacter and Firmicutes used to defne cCCR. The eco- not exhaustive; there are numerous excellent reviews which logical rationale of the reverse diauxie strategy is still an discuss fner aspects of CCR molecular biology [7–12]. open question and is discussed in later sections. The study of cCCR and rCCR has traditionally focused Molecular mechanisms of cCCR on monocultures for the sake of simplicity, possibly limit- ing the interpretation of regulatory systems, as most micro- Gram-negative E. coli utilizes two major cCCR regula- organisms have existed on evolutionary timeframes within tion mechanisms: (1) inducer exclusion [9, 44, 47, 48] consortia [21–24]. The organisms have interacted with other and (2) cyclic AMP (cAMP)-catabolite repressor protein species for millennia, and these interactions have infuenced (CRP) regulation of gene protomer activity; although the access to energy and nutrients [25]. Many genes regulated condition-specifc importance of each mechanism is still an 1 3 398 H. Park et al. Fig. 1 Illustration of classic carbon catabolite repression (cCCR) phenotype with over- fow metabolism and reverse carbon catabolite repression (rCCR) phenotype as well as an illustration of the complemen- tary relationship between the two global metabolism regula- tors. cCCR microorganisms pre- fer glucose to other substrates, while rCCR microorganisms prefer organic acids to glucose open research question [49, 50]. Glucose can enter the cell which generally activates gene targets. The Spot 42 regulon using the multisubunit phosphoenolpyruvate (PEP): carbo- has 29 documented genes [65]. Central metabolism interme- hydrate phosphotransferase system (PTS). Regulation of diates such as a-ketoglutarate, oxaloacetate, PEP, and pyru- cCCR begins with the phosphorylation state of the glucose- vate also play important roles in CCR by afecting the levels specifc subunit of the
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