scholarly journals Mechanistic model of nutrient uptake explains dichotomy between marine oligotrophic and copiotrophic bacteria

2021 ◽  
Vol 17 (5) ◽  
pp. e1009023
Author(s):  
Noele Norris ◽  
Naomi M. Levine ◽  
Vicente I. Fernandez ◽  
Roman Stocker

Marine bacterial diversity is immense and believed to be driven in part by trade-offs in metabolic strategies. Here we consider heterotrophs that rely on organic carbon as an energy source and present a molecular-level model of cell metabolism that explains the dichotomy between copiotrophs—which dominate in carbon-rich environments—and oligotrophs—which dominate in carbon-poor environments—as the consequence of trade-offs between nutrient transport systems. While prototypical copiotrophs, like Vibrios, possess numerous phosphotransferase systems (PTS), prototypical oligotrophs, such as SAR11, lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. We develop models of both transport systems and use them in proteome allocation problems to predict the optimal nutrient uptake and metabolic strategy as a function of carbon availability. We derive a Michaelis–Menten approximation of ABC transport, analytically demonstrating how the half-saturation concentration is a function of binding protein abundance. We predict that oligotrophs can attain nanomolar half-saturation concentrations using binding proteins with only micromolar dissociation constants and while closely matching transport and metabolic capacities. However, our model predicts that this requires large periplasms and that the slow diffusion of the binding proteins limits uptake. Thus, binding proteins are critical for oligotrophic survival yet severely constrain growth rates. We propose that this trade-off fundamentally shaped the divergent evolution of oligotrophs and copiotrophs.

2020 ◽  
Author(s):  
Noele Norris ◽  
Naomi M. Levine ◽  
Vicente I. Fernandez ◽  
Roman Stocker

AbstractMarine heterotrophic bacteria use a spectrum of nutrient uptake strategies, from that of copiotrophs—which dominate in nutrient-rich environments—to that of oligotrophs—which dominate in nutrient-poor environments. While copiotrophs possess numerous phosphotransferase systems (PTS), oligotrophs lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. Here we present a molecular-level model that explains the dichotomy between oligotrophs and copiotrophs as the consequence of trade-offs between PTS and ABC transport. When we approximate ABC transport in Michaelis–Menten form, we find, contrary to the canonical formulation, that its half-saturation concentration KM is not a constant but instead a function of binding protein abundance. Thus, oligotrophs can attain nanomolar KM values using binding proteins with micromolar dissociation constants and while closely matching transport and metabolic capacities. However, this requires large periplasms and high abundances of binding proteins, whose slow diffusion limits uptake rate. We conclude that the use of binding proteins is critical for oligotrophic survival yet severely constrains maximal growth rates, thus fundamentally shaping the divergent evolution of oligotrophs and copiotrophs.


2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Jeroen Meijer ◽  
Bram van Dijk ◽  
Paulien Hogeweg

AbstractMetabolic exchange is widespread in natural microbial communities and an important driver of ecosystem structure and diversity, yet it remains unclear what determines whether microbes evolve division of labor or maintain metabolic autonomy. Here we use a mechanistic model to study how metabolic strategies evolve in a constant, one resource environment, when metabolic networks are allowed to freely evolve. We find that initially identical ancestral communities of digital organisms follow different evolutionary trajectories, as some communities become dominated by a single, autonomous lineage, while others are formed by stably coexisting lineages that cross-feed on essential building blocks. Our results show how without presupposed cellular trade-offs or external drivers such as temporal niches, diverse metabolic strategies spontaneously emerge from the interplay between ecology, spatial structure, and metabolic constraints that arise during the evolution of metabolic networks. Thus, in the long term, whether microbes remain autonomous or evolve metabolic division of labour is an evolutionary contingency.


2011 ◽  
Vol 392 (1-2) ◽  
Author(s):  
Byron C.H. Chu ◽  
Hans J. Vogel

AbstractInEscherichia colithe Fhu, Fep and Fec transport systems are involved in the uptake of chelated ferric iron-siderophore complexes, whereas in pathogenic strains heme can also be used as an iron source. An essential step in these pathways is the movement of the ferric-siderophore complex or heme from the outer membrane transporter across the periplasm to the cognate cytoplasmic membrane ATP-dependent transporter. This is accomplished in each case by a dedicated periplasmic binding protein (PBP). Ferric-siderophore binding PBPs belong to the PBP protein superfamily and adopt a bilobal type III structural fold in which the two independently folded amino and carboxy terminal domains are linked together by a single long α-helix of approximately 20 amino acids. Recent structural studies reveal how the PBPs of the Fhu, Fep, Fec and Chu systems are able to bind their corresponding ligands. These complex structures will be discussed and placed in the context of our current understanding of the entire type III family of Gram-negative periplasmic binding proteins and related Gram-positive substrate binding proteins.


2019 ◽  
Vol 16 (154) ◽  
pp. 20190041 ◽  
Author(s):  
Jonathan Y. Suen ◽  
Saket Navlakha

Both engineered and biological transportation networks face trade-offs in their design. Network users desire to quickly get from one location in the network to another, whereas network planners need to minimize costs in building infrastructure. Here, we use the theory of Pareto optimality to study this design trade-off in the road networks of 101 cities, with wide-ranging population sizes, land areas and geographies. Using a simple one parameter trade-off function, we find that most cities lie near the Pareto front and are significantly closer to the front than expected by alternate design structures. To account for other optimization dimensions or constraints that may be important (e.g. traffic congestion, geography), we performed a higher-order Pareto optimality analysis and found that most cities analysed lie within a region of design space bounded by only four archetypal cities. The trade-offs studied here are also faced and well-optimized by two biological transport networks—neural arbors in the brain and branching architectures of plant shoots—suggesting similar design principles across some biological and engineered transport systems.


2015 ◽  
Author(s):  
Andrea Y. Weisse ◽  
Diego A. Oyarzun ◽  
Vincent Danos ◽  
Peter S. Swain

Intracellular processes rarely work in isolation but continually interact with the rest of the cell. In microbes, for example, we now know that gene expression across the whole genome typically changes with growth rate. The mechanisms driving such global regulation, however, are not well understood. Here we consider three trade-offs that because of limitations in levels of cellular energy, free ribosomes, and proteins are faced by all living cells and construct a mechanistic model that comprises these trade-offs. Our model couples gene expression with growth rate and growth rate with a growing population of cells. We show that the model recovers Monod's law for the growth of microbes and two other empirical relationships connecting growth rate to the mass fraction of ribosomes. Further, we can explain growth related effects in dosage compensation by paralogs and predict host-circuit interactions in synthetic biology. Simulating competitions between strains, we find that the regulation of metabolic pathways may have evolved not to match expression of enzymes to levels of extracellular substrates in changing environments but rather to balance a trade-off between exploiting one type of nutrient over another. Although coarse-grained, the trade-offs that the model embodies are fundamental, and, as such, our modelling framework has potentially wide application, including in both biotechnology and medicine.


2021 ◽  
Vol 288 (1948) ◽  
Author(s):  
Chan Lin ◽  
Henk-Jan T. Hoving ◽  
Thomas W. Cronin ◽  
Karen J. Osborn

Nervous systems across Animalia not only share a common blueprint at the biophysical and molecular level, but even between diverse groups of animals the structure and neuronal organization of several brain regions are strikingly conserved. Despite variation in the morphology and complexity of eyes across malacostracan crustaceans, many studies have shown that the organization of malacostracan optic lobes is highly conserved. Here, we report results of divergent evolution to this ‘neural ground pattern’ discovered in hyperiid amphipods, a relatively small group of holopelagic malacostracan crustaceans that possess an unusually wide diversity of compound eyes. We show that the structure and organization of hyperiid optic lobes has not only diverged from the malacostracan ground pattern, but is also highly variable between closely related genera. Our findings demonstrate a variety of trade-offs between sensory systems of hyperiids and even within the visual system alone, thus providing evidence that selection has modified individual components of the central nervous system to generate distinct combinations of visual centres in the hyperiid optic lobes. Our results provide new insights into the patterns of brain evolution among animals that live under extreme conditions.


2017 ◽  
Author(s):  
Sebastian Funk ◽  
Anton Camacho ◽  
Adam J. Kucharski ◽  
Rachel Lowe ◽  
Rosalind M. Eggo ◽  
...  

AbstractReal-time forecasts based on mathematical models can inform critical decision-making during infectious disease outbreaks. Yet, epidemic forecasts are rarely evaluated during or after the event, and there is little guidance on the best metrics for assessment. Here, we propose an evaluation approach that disentangles different components of forecasting ability using metrics that separately assess the calibration, sharpness and unbiasedness of forecasts. This makes it possible to assess not just how close a forecast was to reality but also how well uncertainty has been quantified. We used this approach to analyse the performance of weekly forecasts we generated in real time in Western Area, Sierra Leone, during the 2013–16 Ebola epidemic in West Africa. We investigated a range of forecast model variants based on the model fits generated at the time with a semi-mechanistic model, and found that good probabilistic calibration was achievable at short time horizons of one or two weeks ahead but models were increasingly inaccurate at longer forecasting horizons. This suggests that forecasts may have been of good enough quality to inform decision making requiring predictions a few weeks ahead of time but not longer, reflecting the high level of uncertainty in the processes driving the trajectory of the epidemic. Comparing forecasts based on the semi-mechanistic model to simpler null models showed that the best semi-mechanistic model variant performed better than the null models with respect to probabilistic calibration, and that this would have been identified from the earliest stages of the outbreak. As forecasts become a routine part of the toolkit in public health, standards for evaluation of performance will be important for assessing quality and improving credibility of mathematical models, and for elucidating difficulties and trade-offs when aiming to make the most useful and reliable forecasts.


2020 ◽  
Vol 142 (12) ◽  
Author(s):  
Ambrosio Valencia-Romero ◽  
Paul T. Grogan

Abstract Strategy dynamics are hypothesized to be a structural factor of interactive multi-actor design problems that influence collective performance and behaviors of design actors. Using a bi-level model of collective decision processes based on design optimization and strategy selection, we formulate a series of two-actor parameter design tasks that exhibit four strategy dynamics (harmony, coexistence, bistability, and defection) associated with low and high levels of structural fear and greed. In these tasks, design actor pairs work collectively to maximize their individual values while managing the trade-offs between aligning with or deviating from a mutually beneficial collective strategy. Results from a human subject design experiment indicate cognizant actors generally follow normative predictions for some strategy dynamics (harmony and coexistence) but not strictly for others (bistability and defection). Cumulative link model regression analysis shows that a greed factor contributing to strategy dynamics has a stronger effect on collective efficiency and equality of individual outcomes compared to a fear factor. Results of this study provide an initial description of strategy dynamics in engineering design and help to frame future work to mitigate potential unfavorable effects of their underlying strategy dynamics through social constructs or mechanism design.


1990 ◽  
Vol 258 (6) ◽  
pp. C1036-C1043 ◽  
Author(s):  
D. J. Pon ◽  
M. Wong ◽  
J. R. Riordan ◽  
B. P. Schimmer

This study characterized the various adenosine 3',5'-cyclic monophosphate (cAMP)-binding proteins in epithelial cells cultured from human sweat glands to identify potential pathways of cAMP action in this tissue. The cAMP-binding proteins were identified by specific labeling with the photoprobe 8-azido-[32P]-cAMP and visualized by autoradiography after electrophoresis on polyacrylamide gels in the presence of sodium dodecyl sulfate. Three cAMP-binding proteins, with molecular masses of 48, 52, and 54 kDa, were identified in subcellular fractions of the cultured sweat glands. On the basis of their relative electrophoretic mobilities and reactivity with specific antisera, the 48-kDa protein was identified as the regulatory subunit of the type 1 cAMP-dependent protein isozyme, and the 54-kDa protein was identified as the regulatory subunit of the type 2 cAMP-dependent protein kinase isozyme. The 52-kDa cAMP-binding protein appeared to be a distinct isoform of the regulatory subunit, possibly related to the subclass associated with neural tissue. As determined from the relative distributions of the photolabel, the 48-, 52-, and 54-kDa binding proteins were present in the cell cytosol at a ratio of 1:2:1. The 48- and 52-kDa proteins bound the photoprobe with apparent dissociation constants (Kd) of 20-40 nM, whereas the 54-kDa protein bound the photoprobe with much lower affinity (Kd 230 nM). Only the 48- and 52-kDa proteins were associated with cell membranes. They were present in the membrane fractions in approximately equal amounts and bound the photoprobe with apparent Kd values of greater than 100 nM.(ABSTRACT TRUNCATED AT 250 WORDS)


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