A network property necessary for concentration robustness

Eloundou-Mbebi, Jeanne M. O.; Küken, Anika; Omranian, Nooshin; Kleeßen, Sabrina; Neigenfind, Jost; Basler, Georg; Nikoloski, Zoran

doi:10.1038/ncomms13255

Cited by 15 publications

(21 citation statements)

References 43 publications

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“…Robustness may be generally defined [8,12,16] as a system-level dynamical property that allows a system to sustain its functions despite changes in internal and external conditions. This feature, in fact, is fundamental and ubiquitous in biological processes, including cellular networks and entire organisms [2,8,12,16].…”

Section: Introductionmentioning

confidence: 99%

A Deficiency-One Algorithm for power-law kinetic systems with reactant-determined interactions

et al. 2018

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Robustness against the presence of environmental disruptions can be observed in many systems of chemical reaction network. However, identifying the underlying components of a system that give rise to robustness is often elusive. The influential work of Shinar and Feinberg established simple yet subtle network-based conditions for absolute concentration robustness (ACR), a phenomena in which a species in a mass-action system has the same concentration for any steady state the network may admit. In this contribution, we extend this result to embrace kinetic systems more general than mass-action systems, namely, powerlaw kinetic systems with reactant-determined interactions (denoted by "PL-RDK"). In PL-RDK, the kinetic order vectors (which we call "interactions") of reactions with the same reactant complex are identical. As illustration, we considered a scenario in the pre-industrial state of global carbon cycle. A power-law approximation of the dynamical system of this scenario is found to be dynamically equivalent to an ACR-possessing PL-RDK system.

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Section: Introductionmentioning

confidence: 99%

A Deficiency-One Algorithm for power-law kinetic systems with reactant-determined interactions

et al. 2018

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“…; Eloundou‐Mbebi et al. ), it is unlikely for carotenoid‐producing networks in birds, given the ancient origin and extraordinary conservation of these networks throughout metazoan evolution. Instead, we suggest that the key structural property of carotenoid networks—biochemical pathway redundancy—allowed for continuity of evolutionary processes operating at vastly different time scales in the species diversifying on this network, empirically illustrating that both robustness and evolvability are necessary conditions for continuous evolution (Maynard Smith ; Gavrilets ; Wagner ; Badyaev ).…”

Section: Discussionmentioning

confidence: 99%

“…It is tempting to speculate that biochemical pathway redundancy, or more generally, the structure of a metabolic network, evolves as a consequence of the most repeatable or efficient flux, when consistent functional priming within generation results in structural redundancy of primed compounds on evolutionary scales. Although this explanation is routinely advanced for evolution of metabolic networks in other systems (Stelling et al 2002;Almaas et al 2005;Ciliberti et al 2007;Kim et al 2007;Basler et al 2016;Eloundou-Mbebi et al 2016), it is unlikely for carotenoidproducing networks in birds, given the ancient origin and extraordinary conservation of these networks throughout metazoan evolution. Instead, we suggest that the key structural property of carotenoid networks-biochemical pathway redundancyallowed for continuity of evolutionary processes operating at vastly different time scales in the species diversifying on this network, empirically illustrating that both robustness and evolvability are necessary conditions for continuous evolution (Maynard Smith 1970;Gavrilets 2004;Wagner 2005;Badyaev 2018).…”

Section: Discussionmentioning

confidence: 99%

Emergent buffering balances evolvability and robustness in the evolution of phenotypic flexibility

Badyaev

Morrison

2018

Evolution

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Evolution of adaptive phenotypic flexibility requires a system that can dynamically restore and update a functional phenotype in response to environmental change. The architecture of such a system evolves under the conflicting demands of versatility and robustness, and resolution of these demands should be particularly evident in organisms that require external inputs for reiterative trait production within a generation, such as in metabolic networks that underlie yearly acquisition of diet-dependent coloration in birds. Here, we show that a key structural feature of carotenoid networks-redundancy of biochemical pathways-enables these networks to translate variable environmental inputs into consistent phenotypic outcomes. We closely followed life-long changes in structure and utilization of metabolic networks in a large cohort of free-living birds and found that greater individual experience with dietary change between molts leads to wider occupancy of the metabolic network and progressive accumulation of redundant pathways in a functionally active network. This generated a regime of emergent buffering whereby greater dietary experience was mechanistically linked to greater robustness of resulting traits and an increasing ability to retain and implement previous adaptive solutions. Thus, experience-related buffering links evolvability and robustness in carotenoid-metabolizing networks and we argue that this mechanistic principle facilitates the evolution of phenotypic flexibility.

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“…Under this scenario, the structure of a metabolic network determines functional properties of metabolism and thus evolves for a specific distribution of flux among compounds (Fig. a; Wagner, ; Eloundou‐Mbebi et al ., ). Adaptive changes in the relative concentrations of compounds produced by metabolic networks would therefore be dependent on the evolution of different network structures, caused by variation in the occurrence of substrate compounds that cannot be metabolically derived (Borenstein et al ., ; Kreimer et al ., ), or the evolution of novel enzymatic reactions and loss of existing reactions (Wagner, ).…”

Section: Introductionmentioning

confidence: 97%

Beyond topology: coevolution of structure and flux in metabolic networks

Morrison

Badyaev

2017

J of Evolutionary Biology

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Interactions between the structure of a metabolic network and its functional properties underlie its evolutionary diversification, but the mechanism by which such interactions arise remains elusive. Particularly unclear is whether metabolic fluxes that determine the concentrations of compounds produced by a metabolic network, are causally linked to a network's structure or emerge independently of it. A direct empirical study of populations where both structural and functional properties vary among individuals' metabolic networks is required to establish whether changes in structure affect the distribution of metabolic flux. In a population of house finches (Haemorhous mexicanus), we reconstructed full carotenoid metabolic networks for 442 individuals and uncovered 11 structural variants of this network with different compounds and reactions. We examined the consequences of this structural diversity for the concentrations of plumage-bound carotenoids produced by flux in these networks. We found that concentrations of metabolically derived, but not dietary carotenoids, depended on network structure. Flux was partitioned similarly among compounds in individuals of the same network structure: within each network, compound concentrations were closely correlated. The highest among-individual variation in flux occurred in networks with the strongest among-compound correlations, suggesting that changes in the magnitude, but not the distribution of flux, underlie individual differences in compound concentrations on a static network structure. These findings indicate that the distribution of flux in carotenoid metabolism closely follows network structure. Thus, evolutionary diversification and local adaptations in carotenoid metabolism may depend more on the gain or loss of enzymatic reactions than on changes in flux within a network structure.

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A network property necessary for concentration robustness

Cited by 15 publications

References 43 publications

A Deficiency-One Algorithm for power-law kinetic systems with reactant-determined interactions

A Deficiency-One Algorithm for power-law kinetic systems with reactant-determined interactions

Emergent buffering balances evolvability and robustness in the evolution of phenotypic flexibility

Beyond topology: coevolution of structure and flux in metabolic networks

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