A general framework of persistence strategies for biological systems helps explain domains of life

Liudmila Sergeevna Mainzer, Monica Wielgos, Suravi Thomas, Arshan Nasir, Minglei Wang, Jay E. Mittenthal, Gustavo Caetano-Anolles

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article numberArticle 16
JournalFrontiers in Genetics
Volume4
Issue numberFEB
DOIs
StatePublished - Apr 19 2013

Fingerprint

Archaea
Optic Disk
Eukaryota
Automatic Data Processing
Reproduction
Fungi
Economics
Bacteria
Costs and Cost Analysis
Growth
Protein Domains

Keywords

  • Economy
  • Flexibility
  • Gap
  • Proteome evolution
  • Redundancy
  • Robustness
  • Scope
  • Umwelt

ASJC Scopus subject areas

  • Molecular Medicine
  • Genetics
  • Genetics(clinical)

Cite this

A general framework of persistence strategies for biological systems helps explain domains of life. / Mainzer, Liudmila Sergeevna; Wielgos, Monica; Thomas, Suravi; Nasir, Arshan; Wang, Minglei; Mittenthal, Jay E.; Caetano-Anolles, Gustavo.

In: Frontiers in Genetics, Vol. 4, No. FEB, Article 16, 19.04.2013.

Research output: Contribution to journalArticle

Mainzer, Liudmila Sergeevna ; Wielgos, Monica ; Thomas, Suravi ; Nasir, Arshan ; Wang, Minglei ; Mittenthal, Jay E. ; Caetano-Anolles, Gustavo. / A general framework of persistence strategies for biological systems helps explain domains of life. In: Frontiers in Genetics. 2013 ; Vol. 4, No. FEB.
@article{5559fbee740b46b8b7f844020f25176a,
title = "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 Uexk{\"u}ll'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.",
keywords = "Economy, Flexibility, Gap, Proteome evolution, Redundancy, Robustness, Scope, Umwelt",
author = "Mainzer, {Liudmila Sergeevna} and Monica Wielgos and Suravi Thomas and Arshan Nasir and Minglei Wang and Mittenthal, {Jay E.} and Gustavo Caetano-Anolles",
year = "2013",
month = "4",
day = "19",
doi = "10.3389/fgene.2013.00016",
language = "English (US)",
volume = "4",
journal = "Frontiers in Genetics",
issn = "1664-8021",
publisher = "Frontiers Media S. A.",
number = "FEB",

}

TY - JOUR

T1 - A general framework of persistence strategies for biological systems helps explain domains of life

AU - Mainzer, Liudmila Sergeevna

AU - Wielgos, Monica

AU - Thomas, Suravi

AU - Nasir, Arshan

AU - Wang, Minglei

AU - Mittenthal, Jay E.

AU - Caetano-Anolles, Gustavo

PY - 2013/4/19

Y1 - 2013/4/19

N2 - 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.

AB - 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.

KW - Economy

KW - Flexibility

KW - Gap

KW - Proteome evolution

KW - Redundancy

KW - Robustness

KW - Scope

KW - Umwelt

UR - http://www.scopus.com/inward/record.url?scp=84876164064&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84876164064&partnerID=8YFLogxK

U2 - 10.3389/fgene.2013.00016

DO - 10.3389/fgene.2013.00016

M3 - Article

VL - 4

JO - Frontiers in Genetics

JF - Frontiers in Genetics

SN - 1664-8021

IS - FEB

M1 - Article 16

ER -