A General Framework of Persistence Strategies for Biological Systems Helps Explain Domains of Life

Abstract

The nature and cause of the division of organisms in superkingdoms is not fully understood. Assuming that environment shapes physiology, here we construct a novel theoretical framework that helps identify general patterns of organism persistence. This framework is based on Jacob von Uexküll’s organism-centric view of the environment and James G. Miller’s view of organisms as matter-energy-information processing molecular machines. Three concepts describe an organism’s environmental niche: scope, umwelt, and gap. Scope denotes the entirety of environmental events and conditions to which the organism is exposed during its lifetime. Umwelt encompasses an organism’s perception of these events. The gap is the organism’s blind spot, the scope that is not covered by umwelt. These concepts bring organisms of different complexity to a common ecological denominator. Ecological and physiological data suggest organisms persist using three strategies: flexibility, robustness, and economy. All organisms use umwelt information to flexibly adapt to environmental change. They implement robustness against environmental perturbations within the gap generally through redundancy and reliability of internal constituents. Both flexibility and robustness improve survival. However, they also incur metabolic matter-energy processing costs, which otherwise could have been used for growth and reproduction. Lineages evolve unique tradeoff solutions among strategies in the space of what we call “a persistence triangle.” Protein domain architecture and other evidence support the preferential use of flexibility and robustness properties. Archaea and Bacteria gravitate toward the triangle’s economy vertex, with Archaea biased toward robustness. Eukarya trade economy for survivability. Protista occupy a saddle manifold separating akaryotes from multicellular organisms. Plants and the more flexible Fungi share an economic stratum, and Metazoa are locked in a positive feedback loop toward flexibility.

Piecemeal Buildup of the Genetic Code, Ribosomes, and Genomes from Primordial tRNA Building Blocks

“…Within these confines, the emerging system exploits the three fundamental properties of any engineered object, economy, flexibility and robustness [15]. Since these properties are strongly impacted by the way the system perceives both the environment and its internal state, the trade-off solutions that are achieved vary with time and context and have been modeled by a “triangle of persistence” and the system’s environmental history, its “scope” [16]. We note that scope has two components, “umwelt” (the system’s perception of that history) and “gap” (the system’s blind spot, the scope that is not covered by its umwelt).…”

Phylogenomics Supports a Cellularly Structured Urancestor

“…The existence of important reductive tendencies in the proteomic repertoires of viruses [ ∼ 3.4 Gy ago; Nasir et al, 2012b] during what we term the 'architectural diversification' epoch of the protein world [Wang et al, 2007] and the onset of reductive tendencies in Archaea ( ∼ 2.9 Gy ago) during the 'superkindom specification' epoch Wang et al, 2007] could provide a rationale for microfossil size variation. Since cell size scales with genome complexity [Yafremava et al, 2013], the small and large kinds of cells may simply represent the cellular ancestors of viruses, the primordial archaeal microbes and the lineage of ancestral bigger cells that gave rise to the two.…”

Long‐term evolution of viruses: A Janus‐faced balance

“…Because of the crucial dependency of viruses to reproduce in an intracellular environment, the three forms of virus‐cell interactions, lysis, latency, and symbiosis are in conflict. Inspired by a previous explanatory framework of trade‐offs of engineering strategies , here we propose that these interactions can lead to propagation , dormancy , and dependency trade‐off solutions fostering flexibility, robustness, and economy (defined in ), respectively, that are beneficial to the long‐term evolution of viruses. This triangle of viral persistence (Fig.…”