Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates

Fares, Hadi M.; Marras, Alexander E.; Ting, Jeffrey M.; Tirrell, Matthew V.; Keating, Christine D.

doi:10.1038/s41467-020-19184-z

Title: Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates

Abstract

Wet-dry cycling on the early Earth is thought to have facilitated production of molecular building blocks of life, but its impact on self-assembly and compartmentalization remains largely unexplored. Here, we investigate dehydration/rehydration of complex coacervates, which are membraneless compartments formed by phase separation of polyelectrolyte solutions. Solution compositions are identified for which tenfold water loss results in maintenance, disappearance, or appearance of coacervate droplets. Systems maintaining coacervates throughout the dehydration process are further evaluated to understand how their compartmentalization properties change with drying. Although added total RNA concentrations increase tenfold, RNA concentration within coacervates remains steady. Exterior RNA concentrations rise, and exchange rates for encapsulated versus free RNAs increase with dehydration. We explain these results in light of the phase diagram, with dehydration-driven ionic strength increase being particularly important in determining coacervate properties. This work shows that wet-dry cycling can alter the phase behavior and protocell-relevant functions of complex coacervates.

Authors:

;

; Tirrell, Matthew V.;

Publication Date:: Tue Oct 27 00:00:00 EDT 2020

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: National Aeronautics and Space Administration (NASA); National Institute of Standards and Technology (NIST); USDOE Office of Science (SC); National Institute of Standards and Technology (NIST), Center for Hierarchical Materials Design (CHiMaD)

OSTI Identifier:: 1690285

Alternate Identifier(s):: OSTI ID: 1815523; OSTI ID: 1840577

Grant/Contract Number:: AC02-06CH11357; 70NANB19H005; 80NSSC17K0034

Resource Type:: Published Article

Journal Name:: Nature Communications

Additional Journal Information:: Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723

Publisher:: Nature Publishing Group

Country of Publication:: United Kingdom

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Chemical origin of life; Physical chemistry; Polymer chemistry; Soft materials

Citation Formats


                    Fares, Hadi M., Marras, Alexander E., Ting, Jeffrey M., Tirrell, Matthew V., and Keating, Christine D. Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates.  United Kingdom: N. p., 2020. 
Web.  doi:10.1038/s41467-020-19184-z.

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                    Fares, Hadi M., Marras, Alexander E., Ting, Jeffrey M., Tirrell, Matthew V., & Keating, Christine D. Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates.  United Kingdom.  https://doi.org/10.1038/s41467-020-19184-z

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                    Fares, Hadi M., Marras, Alexander E., Ting, Jeffrey M., Tirrell, Matthew V., and Keating, Christine D. Tue .  
"Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates".  United Kingdom.  https://doi.org/10.1038/s41467-020-19184-z.

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@article{osti_1690285,

  title        = {Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates},

  author       = {Fares, Hadi M. and Marras, Alexander E. and Ting, Jeffrey M. and Tirrell, Matthew V. and Keating, Christine D.},

  abstractNote = {Wet-dry cycling on the early Earth is thought to have facilitated production of molecular building blocks of life, but its impact on self-assembly and compartmentalization remains largely unexplored. Here, we investigate dehydration/rehydration of complex coacervates, which are membraneless compartments formed by phase separation of polyelectrolyte solutions. Solution compositions are identified for which tenfold water loss results in maintenance, disappearance, or appearance of coacervate droplets. Systems maintaining coacervates throughout the dehydration process are further evaluated to understand how their compartmentalization properties change with drying. Although added total RNA concentrations increase tenfold, RNA concentration within coacervates remains steady. Exterior RNA concentrations rise, and exchange rates for encapsulated versus free RNAs increase with dehydration. We explain these results in light of the phase diagram, with dehydration-driven ionic strength increase being particularly important in determining coacervate properties. This work shows that wet-dry cycling can alter the phase behavior and protocell-relevant functions of complex coacervates.},

  doi          = {10.1038/s41467-020-19184-z},

  journal      = {Nature Communications},

  number       = 1,

  volume       = 11,

  place        = {United Kingdom},

  year         = {Tue Oct 27 00:00:00 EDT 2020},

  month        = {Tue Oct 27 00:00:00 EDT 2020}

}

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Title: Impact of wet-dry cycling on the phase behavior and compartmentalization properties of complex coacervates

Abstract

Citation Formats

Scattering Neutrons along the Polyelectrolyte Complex/Coacervate Continuum journal, June 2018

Diffusion of Sites versus Polymers in Polyelectrolyte Complexes and Multilayers journal, October 2017

Characteristic lengths and the structure of salt free polyelectrolyte solutions. A small angle neutron scattering study journal, December 1985

Phase behaviour and complex coacervation of aqueous polypeptide solutions journal, January 2012

Origin of first cells at terrestrial, anoxic geothermal fields journal, February 2012

Aqueous Phase Separation as a Possible Route to Compartmentalization of Biological Molecules journal, February 2012

Catalysts for the self-polymerization of adenosine cyclic 2′,3′-phosphate journal, December 1973

Molecular and structural basis of low interfacial energy of complex coacervates in water journal, January 2017

Viscosity and interfacial properties in a mussel-inspired adhesive coacervate journal, January 2010

Peptide–nucleotide microdroplets as a step towards a membrane-free protocell model journal, August 2011

In vitro gene expression within membrane-free coacervate protocells journal, January 2015

Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions journal, May 1982

Reversible generation of coacervate droplets in an enzymatic network journal, January 2018

Ester-Mediated Amide Bond Formation Driven by Wet-Dry Cycles: A Possible Path to Polypeptides on the Prebiotic Earth journal, July 2015

Origin of life: The RNA world journal, February 1986

Non-equilibrium behaviour in coacervate-based protocells under electric-field-induced excitation journal, February 2016

The Effect of Limited Diffusion and Wet–Dry Cycling on Reversible Polymerization Reactions: Implications for Prebiotic Synthesis of Nucleic Acids journal, June 2016

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Thermal synthesis and hydrolysis of polyglyceric acid journal, January 1989

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Molecular weight fractionation and the self-suppression of complex coacervation journal, January 1967

Partitioning and Enhanced Self-Assembly of Actin in Polypeptide Coacervates journal, April 2018

50th Anniversary Perspective : A Perspective on Polyelectrolyte Solutions journal, December 2017

Phase Behavior and Salt Partitioning in Polyelectrolyte Complex Coacervates journal, April 2018

The Hot Spring Hypothesis for an Origin of Life journal, April 2020

Protein/polysaccharide complexes and coacervates in food systems journal, September 2011

Coupled Phases and Combinatorial Selection in Fluctuating Hydrothermal Pools: A Scenario to Guide Experimental Approaches to the Origin of Cellular Life journal, March 2015

Complex coacervates as a foundation for synthetic underwater adhesives journal, September 2011

Phase Behavior and Coacervation of Aqueous Poly(acrylic acid)−Poly(allylamine) Solutions journal, March 2010

Complex coacervate core micelles journal, March 2009

Polyanion-Assisted Ribozyme Catalysis Inside Complex Coacervates journal, May 2019

Wet-dry cycles enable the parallel origin of canonical and non-canonical nucleosides by continuous synthesis journal, January 2018

Microfluidic Formation of Monodisperse Coacervate Organelles in Liposomes journal, July 2017

Approximations Leading to a Unified Exponential/Power-Law Approach to Small-Angle Scattering journal, December 1995

Phase Diagrams of the Aqueous Two-Phase Systems of Poly(ethylene glycol)/Sodium Polyacrylate/Salts journal, March 2011

Rapid RNA Exchange in Aqueous Two-Phase System and Coacervate Droplets journal, February 2014

Prebiotic condensation through wet–dry cycling regulated by deliquescence journal, October 2019

Microfluidic Formation of Membrane-Free Aqueous Coacervate Droplets in Water journal, May 2015

pH-Induced Coacervation in Complexes of Bovine Serum Albumin and Cationic Polyelectrolytes journal, March 2000

The Origin of RNA and “My Grandfather’s Axe” journal, April 2013

Compartmentalised RNA catalysis in membrane-free coacervate protocells journal, September 2018

Coacervate delivery systems for proteins and small molecule drugs journal, August 2014

Diffusion and Electrophoretic Mobility of Single-Stranded RNA from Molecular Dynamics Simulations journal, February 2004

Salt-Promoted Synthesis of RNA-like Molecules in Simulated Hydrothermal Conditions journal, December 2014

Dry/Wet Cycling and the Thermodynamics and Kinetics of Prebiotic Polymer Synthesis journal, July 2016

Ion-Pairing Strength in Polyelectrolyte Complexes journal, January 2017

Structure and Dynamics of Polyelectrolyte Complex Coacervates Studied by Scattering of Neutrons, X-rays, and Light journal, May 2013

Peptide formation in the prebiotic era: thermal condensation of glycine in fluctuating clay environments journal, July 1978

Molecular Origin of the Glass Transition in Polyelectrolyte Assemblies journal, April 2018

RNA-Based Coacervates as a Model for Membraneless Organelles: Formation, Properties, and Interfacial Liposome Assembly journal, September 2016

Biomolecular condensates: organizers of cellular biochemistry journal, February 2017

Quantifying Dynamics in Phase-Separated Condensates Using Fluorescence Recovery after Photobleaching journal, October 2019

Membraneless organelles can melt nucleic acid duplexes and act as biomolecular filters journal, May 2016

Sequence and entropy-based control of complex coacervates journal, November 2017

Mobility measurement by analysis of fluorescence photobleaching recovery kinetics journal, September 1976

Programming molecular self-assembly of intrinsically disordered proteins containing sequences of low complexity journal, January 2017

Formation and Stability of Prebiotically Relevant Vesicular Systems in Terrestrial Geothermal Environments journal, November 2017

Ester Formation and Hydrolysis during Wet–Dry Cycles: Generation of Far-from-Equilibrium Polymers in a Model Prebiotic Reaction journal, February 2014

Formation of oligopeptides in high yield under simple programmable conditions journal, October 2015

Scattering Neutrons along the Polyelectrolyte Complex/Coacervate Continuum
journal, June 2018

Diffusion of Sites versus Polymers in Polyelectrolyte Complexes and Multilayers
journal, October 2017

Characteristic lengths and the structure of salt free polyelectrolyte solutions. A small angle neutron scattering study
journal, December 1985

Phase behaviour and complex coacervation of aqueous polypeptide solutions
journal, January 2012

Origin of first cells at terrestrial, anoxic geothermal fields
journal, February 2012

Aqueous Phase Separation as a Possible Route to Compartmentalization of Biological Molecules
journal, February 2012

Catalysts for the self-polymerization of adenosine cyclic 2′,3′-phosphate
journal, December 1973

Molecular and structural basis of low interfacial energy of complex coacervates in water
journal, January 2017

Viscosity and interfacial properties in a mussel-inspired adhesive coacervate
journal, January 2010

Peptide–nucleotide microdroplets as a step towards a membrane-free protocell model
journal, August 2011

In vitro gene expression within membrane-free coacervate protocells
journal, January 2015

Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions
journal, May 1982

Reversible generation of coacervate droplets in an enzymatic network
journal, January 2018

Ester-Mediated Amide Bond Formation Driven by Wet-Dry Cycles: A Possible Path to Polypeptides on the Prebiotic Earth
journal, July 2015

Origin of life: The RNA world
journal, February 1986

Non-equilibrium behaviour in coacervate-based protocells under electric-field-induced excitation
journal, February 2016

The Effect of Limited Diffusion and Wet–Dry Cycling on Reversible Polymerization Reactions: Implications for Prebiotic Synthesis of Nucleic Acids
journal, June 2016

An automated apparatus for the simulation of prebiotic wet‒dry cycles under strictly anaerobic conditions
journal, February 2018

Thermal synthesis and hydrolysis of polyglyceric acid
journal, January 1989

The Polyelectrolyte Complex/Coacervate Continuum
journal, April 2014

Thermal Copolymerization of Amino Acids to a Product Resembling Protein
journal, November 1958

Irena : tool suite for modeling and analysis of small-angle scattering
journal, February 2009

Phosphorylation-mediated RNA/peptide complex coacervation as a model for intracellular liquid organelles
journal, December 2015

Polyamine/Nucleotide Coacervates Provide Strong Compartmentalization of Mg ²⁺ , Nucleotides, and RNA
journal, February 2016

Lipid-assisted Synthesis of RNA-like Polymers from Mononucleotides
journal, November 2007

Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates
journal, January 2019

Molecular weight fractionation and the self-suppression of complex coacervation
journal, January 1967

Partitioning and Enhanced Self-Assembly of Actin in Polypeptide Coacervates
journal, April 2018

50th Anniversary Perspective : A Perspective on Polyelectrolyte Solutions
journal, December 2017

Phase Behavior and Salt Partitioning in Polyelectrolyte Complex Coacervates
journal, April 2018

The Hot Spring Hypothesis for an Origin of Life
journal, April 2020

Protein/polysaccharide complexes and coacervates in food systems
journal, September 2011

Coupled Phases and Combinatorial Selection in Fluctuating Hydrothermal Pools: A Scenario to Guide Experimental Approaches to the Origin of Cellular Life
journal, March 2015

Complex coacervates as a foundation for synthetic underwater adhesives
journal, September 2011

Phase Behavior and Coacervation of Aqueous Poly(acrylic acid)−Poly(allylamine) Solutions
journal, March 2010

Complex coacervate core micelles
journal, March 2009

Polyanion-Assisted Ribozyme Catalysis Inside Complex Coacervates
journal, May 2019

Wet-dry cycles enable the parallel origin of canonical and non-canonical nucleosides by continuous synthesis
journal, January 2018

Microfluidic Formation of Monodisperse Coacervate Organelles in Liposomes
journal, July 2017

Approximations Leading to a Unified Exponential/Power-Law Approach to Small-Angle Scattering
journal, December 1995

Phase Diagrams of the Aqueous Two-Phase Systems of Poly(ethylene glycol)/Sodium Polyacrylate/Salts
journal, March 2011

Rapid RNA Exchange in Aqueous Two-Phase System and Coacervate Droplets
journal, February 2014

Prebiotic condensation through wet–dry cycling regulated by deliquescence
journal, October 2019

Microfluidic Formation of Membrane-Free Aqueous Coacervate Droplets in Water
journal, May 2015

pH-Induced Coacervation in Complexes of Bovine Serum Albumin and Cationic Polyelectrolytes
journal, March 2000

The Origin of RNA and “My Grandfather’s Axe”
journal, April 2013

Compartmentalised RNA catalysis in membrane-free coacervate protocells
journal, September 2018

Coacervate delivery systems for proteins and small molecule drugs
journal, August 2014

Diffusion and Electrophoretic Mobility of Single-Stranded RNA from Molecular Dynamics Simulations
journal, February 2004

Salt-Promoted Synthesis of RNA-like Molecules in Simulated Hydrothermal Conditions
journal, December 2014

Dry/Wet Cycling and the Thermodynamics and Kinetics of Prebiotic Polymer Synthesis
journal, July 2016

Ion-Pairing Strength in Polyelectrolyte Complexes
journal, January 2017

Structure and Dynamics of Polyelectrolyte Complex Coacervates Studied by Scattering of Neutrons, X-rays, and Light
journal, May 2013

Peptide formation in the prebiotic era: thermal condensation of glycine in fluctuating clay environments
journal, July 1978

Molecular Origin of the Glass Transition in Polyelectrolyte Assemblies
journal, April 2018

RNA-Based Coacervates as a Model for Membraneless Organelles: Formation, Properties, and Interfacial Liposome Assembly
journal, September 2016

Biomolecular condensates: organizers of cellular biochemistry
journal, February 2017

Quantifying Dynamics in Phase-Separated Condensates Using Fluorescence Recovery after Photobleaching
journal, October 2019

Membraneless organelles can melt nucleic acid duplexes and act as biomolecular filters
journal, May 2016

Sequence and entropy-based control of complex coacervates
journal, November 2017

Mobility measurement by analysis of fluorescence photobleaching recovery kinetics
journal, September 1976

Programming molecular self-assembly of intrinsically disordered proteins containing sequences of low complexity
journal, January 2017

Formation and Stability of Prebiotically Relevant Vesicular Systems in Terrestrial Geothermal Environments
journal, November 2017

Ester Formation and Hydrolysis during Wet–Dry Cycles: Generation of Far-from-Equilibrium Polymers in a Model Prebiotic Reaction
journal, February 2014

Formation of oligopeptides in high yield under simple programmable conditions
journal, October 2015