Environmental boundary conditions for the origin of life converge to an organo-sulfur metabolism

Published in final edited form as: Nat Ecol Evol. 2019 December ; 3(12): 1715–1724. doi:10.1038/s41559-019-1018-8.It has been suggested that a deep memory of early life is hidden in the architecture of metabolic networks, whose reactions could have been catalyzed by small molecules or minerals before genetically encoded enzymes. A major challenge in unravelling these early steps is assessing the plausibility of a connected, thermodynamically consistent proto-metabolism under different geochemical conditions, which are still surrounded by high uncertainty. Here we combine network-based algorithms with physico-chemical constraints on chemical reaction networks to systematically show how different combinations of parameters (temperature, pH, redox potential and availability of molecular precursors) could have affected the evolution of a proto-metabolism. Our analysis of possible trajectories indicates that a subset of boundary conditions converges to an organo-sulfur-based proto-metabolic network fuelled by a thioester- and redox-driven variant of the reductive tricarboxylic acid cycle that is capable of producing lipids and keto acids. Surprisingly, environmental sources of fixed nitrogen and low-potential electron donors are not necessary for the earliest phases of biochemical evolution. We use one of these networks to build a steady-state dynamical metabolic model of a protocell, and find that different combinations of carbon sources and electron donors can support the continuous production of a minimal ancient 'biomass' composed of putative early biopolymers and fatty acids.80NSSC17K0295 - Intramural NASA; 80NSSC17K0296 - Intramural NASA; T32 GM100842 - NIGMS NIH HHSAccepted manuscrip

The white-knight hypothesis, or does the environment limit innovations?

Organisms often harbor latent traits that are byproducts of other adaptations. Such latent traits are not themselves adaptive but can become adaptive in the right environment. Here I discuss several examples of such traits. Their abundance suggests that environmental change rather than new mutations might often limit the origin of evolutionary adaptations and innovations. This is important, because environments can change much faster than new mutations arise. I introduce a conceptual model that distinguishes between mutation-limited and environment-limited trait origins and suggest how experiments could help discriminate between them. Wherever latent traits are plentiful, ecology rather than genetics might determine how fast new adaptations originate and thus how fast adaptive Darwinian evolution proceeds

The compositional and evolutionary logic of metabolism

Metabolism displays striking and robust regularities in the forms of modularity and hierarchy, whose composition may be compactly described. This renders metabolic architecture comprehensible as a system, and suggests the order in which layers of that system emerged. Metabolism also serves as the foundation in other hierarchies, at least up to cellular integration including bioenergetics and molecular replication, and trophic ecology. The recapitulation of patterns first seen in metabolism, in these higher levels, suggests metabolism as a source of causation or constraint on many forms of organization in the biosphere. We identify as modules widely reused subsets of chemicals, reactions, or functions, each with a conserved internal structure. At the small molecule substrate level, module boundaries are generally associated with the most complex reaction mechanisms and the most conserved enzymes. Cofactors form a structurally and functionally distinctive control layer over the small-molecule substrate. Complex cofactors are often used at module boundaries of the substrate level, while simpler ones participate in widely used reactions. Cofactor functions thus act as "keys" that incorporate classes of organic reactions within biochemistry. The same modules that organize the compositional diversity of metabolism are argued to have governed long-term evolution. Early evolution of core metabolism, especially carbon-fixation, appears to have required few innovations among a small number of conserved modules, to produce adaptations to simple biogeochemical changes of environment. We demonstrate these features of metabolism at several levels of hierarchy, beginning with the small-molecule substrate and network architecture, continuing with cofactors and key conserved reactions, and culminating in the aggregation of multiple diverse physical and biochemical processes in cells.Comment: 56 pages, 28 figure

Think tank: water relations of Bromeliaceae in their evolutionary context

This is the final version of the article. It first appeared from Wiley via https://doi.org/10.1111/boj.12423Water relations represent a pivotal nexus in plant biology due to the multiplicity of functions affected by water status. Hydraulic properties of plant parts are therefore likely to be relevant to evolutionary trends in many taxa. Bromeliaceae encompass a wealth of morphological, physiological and ecological variations and the geographical and bioclimatic range of the family is also extensive. The diversification of bromeliad lineages is known to be correlated with the origins of a suite of key innovations, many of which relate directly or indirectly to water relations. However, little information is known regarding the role of change in morphoanatomical and hydraulic traits in the evolutionary origins of the classical ecophysiological functional types in Bromeliaceae or how this role relates to the diversification of specific lineages. In this paper, I present a synthesis of the current knowledge on bromeliad water relations and a qualitative model of the evolution of relevant traits in the context of the functional types. I use this model to introduce a manifesto for a new research programme on the integrative biology and evolution of bromeliad water-use strategies. The need for a wide-ranging survey of morphoanatomical and hydraulic traits across Bromeliaceae is stressed, as this would provide extensive insight into structure–function relationships of relevance to the evolutionary history of bromeliads and, more generally, to the evolutionary physiology of flowering plants.Natural Environment Research Counci

Power, competition, and the nature of history

AbstractHistorians have debated whether pathways and events from the past to the present are influenced largely by contingency, the dependence of outcomes on particular prior conditions, or whether there is long-term emergent directional change. Previous arguments for predictability in evolutionary history relied on the high frequency of convergence, but the repeated evolution of widely favored adaptations need not imply long-term directionality. Using evidence from the fossil record and arguments concerning the metabolic evolution of organisms, I show here that power (total energy taken up and expended per unit time) has increased stepwise over time at ecosystem-level and global scales thanks to the ratchet-like, cumulative effects of competition and cooperation and to the disproportionate influence of powerful top competitors and opportunistic species on emergent ecosystem properties and processes. The history of life therefore exhibits emergent directionality at large ecosystem-wide scales toward greater power

Network-level architecture and the evolutionary potential of underground metabolism

A central unresolved issue in evolutionary biology is how metabolic innovations emerge. Low-level enzymatic side activities are frequent and can potentially be recruited for new biochemical functions. However, the role of such underground reactions in adaptation toward novel environments has remained largely unknown and out of reach of computational predictions, not least because these issues demand analyses at the level of the entire metabolic network. Here, we provide a comprehensive computational model of the underground metabolism in Escherichia coli. Most underground reactions are not isolated and 45% of them can be fully wired into the existing network and form novel pathways that produce key precursors for cell growth. This observation allowed us to conduct an integrated genome-wide in silico and experimental survey to characterize the evolutionary potential of E. coli to adapt to hundreds of nutrient conditions. We revealed that underground reactions allow growth in new environments when their activity is increased. We estimate that at least similar to 20% of the underground reactions that can be connected to the existing network confer a fitness advantage under specific environments. Moreover, our results demonstrate that the genetic basis of evolutionary adaptations via underground metabolism is computationally predictable. The approach used here has potential for various application areas from bioengineering to medical genetics

Genomic Inference of the Metabolism and Evolution of the Archaeal Phylum Aigarchaeota

Microbes of the phylum Aigarchaeota are widely distributed in geothermal environments, but their physiological and ecological roles are poorly understood. Here we analyze six Aigarchaeota metagenomic bins from two circumneutral hot springs in Tengchong, China, to reveal that they are either strict or facultative anaerobes, and most are chemolithotrophs that can perform sulfide oxidation. Applying comparative genomics to the Thaumarchaeota and Aigarchaeota, we find that they both originated from thermal habitats, sharing 1154 genes with their common ancestor. Horizontal gene transfer played a crucial role in shaping genetic diversity of Aigarchaeota and led to functional partitioning and ecological divergence among sympatric microbes, as several key functional innovations were endowed by Bacteria, including dissimilatory sulfite reduction and possibly carbon monoxide oxidation. Our study expands our knowledge of the possible ecological roles of the Aigarchaeota and clarifies their evolutionary relationship to their sister lineage Thaumarchaeota

Metabolic evolution and the self-organization of ecosystems

Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and self-organization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen.Simons Foundation (Grant SCOPE 329108)Gordon and Betty Moore Foundation (Grant 3778)Gordon and Betty Moore Foundation (Grant 495.01

Human metabolic adaptations and prolonged expensive neurodevelopment: A review

1.	After weaning, human hunter-gatherer juveniles receive substantial (≈3.5-7 MJ day^-1^), extended (≈15 years) and reliable (kin and nonkin food pooling) energy provision.
2.	The childhood (pediatric) and the adult human brain takes a very high share of both basal metabolic rate (BMR) (child: 50-70%; adult: ≈20%) and total energy expenditure (TEE) (child: 30-50%; adult: ≈10%).
3.	The pediatric brain for an extended period (≈4-9 years-of-age) consumes roughly 50% more energy than the adult one, and after this, continues during adolescence, at a high but declining rate. Within the brain, childhood cerebral gray matter has an even higher 1.9 to 2.2-fold increased energy consumption. 
4.	This metabolic expensiveness is due to (i) the high cost of synapse activation (74% of brain energy expenditure in humans), combined with (ii), a prolonged period of exuberance in synapse numbers (up to double the number present in adults). Cognitive development during this period associates with volumetric changes in gray matter (expansion and contraction due to metabolic related size alterations in glial cells and capillary vascularization), and in white matter (expansion due to myelination). 
5.	Amongst mammals, anatomically modern humans show an unique pattern in which very slow musculoskeletal body growth is followed by a marked adolescent size/stature spurt. This pattern of growth contrasts with nonhuman primates that have a sustained fast juvenile growth with only a minor period of puberty acceleration. The existence of slow childhood growth in humans has been shown to date back to 160,000 BP. 
6.	Human children physiologically have a limited capacity to protect the brain from plasma glucose fluctuations and other metabolic disruptions. These can arise in adults, during prolonged strenuous exercise when skeletal muscle depletes plasma glucose, and produces other metabolic disruptions upon the brain (hypoxia, hyperthermia, dehydration and hyperammonemia). These are proportional to muscle mass.
7.	Children show specific adaptations to minimize such metabolic disturbances. (i) Due to slow body growth and resulting small body size, they have limited skeletal muscle mass. (ii) They show other adaptations such as an exercise specific preference for free fatty acid metabolism. (iii) While children are generally more active than adolescents and adults, they avoid physically prolonged intense exertion. 
8.	Childhood has a close relationship to high levels of energy provision and metabolic adaptations that support prolonged synaptic neurodevelopment. 
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Economic resilience : including a case study of the global transition network

This paper explores the dynamic properties of organisms and ecosystems that make them so resilient and capable of adapting to changing circumstances, allowing them to maintain an overall condition of coherence, wholeness and health while living in balance within the resources of the planet. Key principles of resilient ecological systems are explored including: self-regulation; positive and negative feedback; diversity; scale and context; cooperation; emergence and novelty; and ecological tipping points. In contrast, market based economic systems can produce unstable growth with unintended destruction of cultural and species diversity and homogenisation of global life-styles. The paper re-examines fundamental economic principles using insights from biological evolution and ecosystem dynamics to establish a foundation for more resilient economies. This involves experimenting with different models in different communities to find patterns of sustainable production and exchange appropriate to local regions. Fundamental steps in this direction include the emergence of self-organising local communities based on creative experimentation, re-localisation of core sectors of the economy (food, energy, health and education), evolution of local currencies and banking practices that support local enterprise and investment in green technologies, stimulation of decentralised renewable energy networks and economic reform aligned with ecological principles. The Transition Network provides a case study of an international community based movement that has been experimenting with putting some of these principles into practice at the local level. The aim of the Transition Network is to support community led responses to peak oil and climate change, building resilience and well-being. The concept of ecological resilience and its application to local economy is hard wired into the values and emerging structure of the network of transition communities across the globe. The movement started in the UK in 2005 and there are now over 1000 Transition initiatives spanning 34 countries across the world. Many attribute the success and phenomenal growth of the Transition Network to its emerging holographic structure that mimics cell growth within living organisms. Growing a more resilient food system in the face of the twin challenges of natural resource scarcity and climate change is central to the Transition movement. A set of principles for a post carbon resilient food economy in the UK are offered. These include an 80% cut in carbon emission in the food sector by 2050, agricultural diversification, prioritization of farming methods that establish and enhance carbon sinks, phasing out of dependence on fossil fuels in food growing, processing and distribution, promoting access to nutritious and affordable food, as well as promoting greater access to land for growing food in urban and peri-urban areas. Practical examples of Transition related projects in the food sector are presented across the following themes: access to land, low carbon production methods, food distribution systems, health and community gardens and orchards, and collaborative ownership models