Behavioral metabolution: the adaptive and evolutionary potential of metabolism-based chemotaxis

We use a minimal model of metabolism-based chemotaxis to show how a coupling between metabolism and behavior can affect evolutionary dynamics in a process we refer to as behavioral metabolution. This mutual influence can function as an in-the-moment, intrinsic evaluation of the adaptive value of a novel situation, such as an encounter with a compound that activates new metabolic pathways. Our model demonstrates how changes to metabolic pathways can lead to improvement of behavioral strategies, and conversely, how behavior can contribute to the exploration and fixation of new metabolic pathways. These examples indicate the potentially important role that the interplay between behavior and metabolism could have played in shaping adaptive evolution in early life and protolife. We argue that the processes illustrated by these models can be interpreted as an unorthodox instantiation of the principles of evolution by random variation and selective retention. We then discuss how the interaction between metabolism and behavior can facilitate evolution through (i) increasing exposure to environmental variation, (ii) making more likely the fixation of some beneficial metabolic pathways, (iii) providing a mechanism for in-the-moment adaptation to changes in the environment and to changes in the organization of the organism itself, and (iv) generating conditions that are conducive to speciatio

Systems-chemistry approach to prebiotic evolution

The puzzle of the origin of life is grand. A major challenge is to understand the transition from a mixture of molecules into an entity with basic life faculties, such as a protocell, capable of self-replication and inheritance. Two major schools tackle this problem: the genetic, or replicator-first approach, and the metabolism-first approach. The replicator-first approach focuses on a single self-perpetuating informational biopolymer, e.g., RNA, as the first step, and it is thus often referred to as the “RNA world”. In contrast, the metabolism-first approach focuses on a network of chemical reactions among simpler chemical components that became endowed with some reproductive characteristics as the first step that led to a protocell. The lipid world scenario, largely initiated by our laboratory, delineates a specific example of metabolism first. It suggests that spontaneously forming assemblies of relatively simple molecules, such as mutually interacting lipids, that resemble primitive metabolism, are capable of storing and transmitting information similar to sequence-based polymeric RNA, except that in this case it is compositional information that is at work. This thesis is about further exploration of the lipid world scenario, showing in more detail how a relatively simple chemical system can acquire features such as selection and evolution. This was accomplished by studying dynamical aspects of the graded autocatalysis replication domain (GARD) computer-simulation lipid world model, previously developed at our laboratory. GARD simulates the homeostatic growth of a compositional amphiphile assembly by reversible accretion from a buffered heterogeneous external pool. This process is governed by a network of mutually catalytic reactions, and exhibits quasi-stationary compositional states termed compotype, that may be regarded as GARD species. I have demonstrated that that such GARD species exhibit positive as well as negative selection, an important prerequisite of a minimally living system. I further showed that when the catalytic network becomes dominated by mutual catalysis, as opposed to self-catalysis, selection is enhanced. When studying the dynamics of large populations of GARD assemblies under constant population conditions, I rewardingly found that they exhibit dynamics similar to natural ecosystem populations, e.g. similes of competition or predator-prey dynamics. I was able to establish relationships between a compotype’s internal molecular parameters (e.g. its molecular diversity) and population ecology behavior. In a separate vein, I have developed a new approach towards observing open-ended evolution, which enables asking whether there is an optimal level of open endedness in prebiotic evolution. Finally, I was able to show clear similarities between GARD compotypes and quasispecies in the Eigen-Schuster model for evolution, further underlining GARD’s capacity as an alternative to RNA World. Taken together, these results uncover quantitative aspects of the GARD model which in turn contribute towards our understanding of the origin of life via the lipid world scenario

Analysis of minimal metabolic networks through whole-cell in silico modelling of prokaryotes

Tese de Mestrado Integrado. Bioengenharia. Faculdade de Engenharia. Universidade do Porto. 201

Adaptation from interactions between metabolism and behaviour: self-sensitive behaviour in protocells

This thesis considers the relationship between adaptive behaviour and metabolism, using theoretical arguments supported by computational models to demonstrate mechanisms of adaptation that are uniquely available to systems based upon the metabolic organisation of self-production. It is argued how, by being sensitive to their metabolic viability, an organism can respond to the quality of its environment with respect to its metabolic well-being. This makes possible simple but powerful ‘self-sensitive’ adaptive behaviours such as “If I am healthy now, keep doing the same as I have been doing – otherwise do something else.” This strategy provides several adaptive benefits, including the ability to respond appropriately to phenomena never previously experienced by the organism nor by any of its ancestors; the ability to integrate different environmental influences to produce an appropriate response; and sensitivity to the organism’s present context and history of experience. Computational models are used to demonstrate these capabilities, as well as the possibility that self-sensitive adaptive behaviour can facilitate the adaptive evolution of populations of self-sensitive organisms through (i) processes similar to the Baldwin effect, (ii) increasing the likelihood of speciation events, and (iii) automatic behavioural adaptation to changes in the organism itself (such as genetic changes). In addition to these theoretical contributions, a computational model of self-sensitive behaviour is presented that recreates chemotaxis patterns observed in bacteria such as Azospirillum brasilense and Campylobacter jejuni. The models also suggest new explanations for previously unexplained asymmetric distributions of bacteria performing aerotaxis. More broadly, the work advocates further research into the relationship between behaviour and the metabolic organisation of self-production, an organisational property shared by all life. It also acts as an example of how abstract models that target theoretical concepts rather than natural phenomena can play a valuable role in the scientific endeavour

Systems protobiology:Origin of life in lipid catalytic networks

Life is that which replicates and evolves, but there is no consensus on how life emerged. We advocate a systems protobiology view, whereby the first replicators were assemblies of spontaneously accreting, heterogeneous and mostly non-canonical amphiphiles. This view is substantiated by rigorous chemical kinetics simulations of the graded autocatalysis replication domain (GARD) model, based on the notion that the replication or reproduction of compositional information predated that of sequence information. GARD reveals the emergence of privileged non-equilibrium assemblies (composomes), which portray catalysis-based homeostatic (concentration-preserving) growth. Such a process, along with occasional assembly fission, embodies cell-like reproduction. GARD pre-RNA evolution is evidenced in the selection of different composomes within a sparse fitness landscape, in response to environmental chemical changes. These observations refute claims that GARD assemblies (or other mutually catalytic networks in the metabolism first scenario) cannot evolve. Composomes represent both a genotype and a selectable phenotype, anteceding present-day biology in which the two are mostly separated. Detailed GARD analyses show attractor-like transitions from random assemblies to self-organized composomes, with negative entropy change, thus establishing composomes as dissipative systemstextemdashhallmarks of life. We show a preliminary new version of our model, metabolic GARD (M-GARD), in which lipid covalent modifications are orchestrated by non-enzymatic lipid catalysts, themselves compositionally reproduced. M-GARD fills the gap of the lack of true metabolism in basic GARD, and is rewardingly supported by a published experimental instance of a lipid-based mutually catalytic network. Anticipating near-future far-reaching progress of molecular dynamics, M-GARD is slated to quantitatively depict elaborate protocells, with orchestrated reproduction of both lipid bilayer and lumenal content. Finally, a GARD analysis in a whole-planet context offers the potential for estimating the probability of life's emergence. The invigorated GARD scrutiny presented in this review enhances the validity of autocatalytic sets as a bona fide early evolution scenario and provides essential infrastructure for a paradigm shift towards a systems protobiology view of life's origin

A complex systems approach to education in Switzerland

The insights gained from the study of complex systems in biological, social, and engineered systems enables us not only to observe and understand, but also to actively design systems which will be capable of successfully coping with complex and dynamically changing situations. The methods and mindset required for this approach have been applied to educational systems with their diverse levels of scale and complexity. Based on the general case made by Yaneer Bar-Yam, this paper applies the complex systems approach to the educational system in Switzerland. It confirms that the complex systems approach is valid. Indeed, many recommendations made for the general case have already been implemented in the Swiss education system. To address existing problems and difficulties, further steps are recommended. This paper contributes to the further establishment complex systems approach by shedding light on an area which concerns us all, which is a frequent topic of discussion and dispute among politicians and the public, where billions of dollars have been spent without achieving the desired results, and where it is difficult to directly derive consequences from actions taken. The analysis of the education system's different levels, their complexity and scale will clarify how such a dynamic system should be approached, and how it can be guided towards the desired performance

Early Systems Biology and Prebiotic Networks

Abstract. Systems Biology constitutes tools and approaches aimed at deciphering complex biological entities. It is assumed that such complexity arose gradually, beginning from a few relatively simple molecules at life’s inception, and culminating with the emergence of composite multicellular organisms billions of years later. The main point of the present paper is that very early in the evolution of life, molecular ensembles with high complexity may have arisen, which are best described and analyzed by the tools of Systems Biology. We show that modeled prebiotic mutually catalytic pathways have network attributes similar to those of present-day living cells. This includes network motifs and robustness attributes. We point out that early networks are weighted (graded), but that using a cutoff formalism one may probe their degree distribution and show that it approximate that of a random network. A question is then posed regarding the potential evolutionary mechanisms that may have led to the emergence of scale-free networks in modern cells. 1 Prebiotic Molecular Network