Membranous and Membraneless Interfaces—Origins of Artificial Cellular Complexity

A special issue of Life (ISSN 2075-1729). This special issue belongs to the section "Synthetic Biology and Systems Biology".

Deadline for manuscript submissions: closed (31 May 2022) | Viewed by 14622

Special Issue Editors


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Guest Editor
Dipartimento di Scienze e Tecnologie Biologiche e Ambientali (DiSTeBA), Università del Salento Campus Ecotekne, S.P. 6 Lecce-Monteroni, 73100 Lecce, Italy
Interests: origins of life; synthetic biology; artificial life; synthetic cells; drug delivery; bio-chem-ICTs; autopoiesis and cognition
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Guest Editor
Division of Chemistry for Materials, Graduate School of Engineering, Mie University, Tsu, Mie 514-8507, Japan
Interests: artificial membranes; liposomes; biological phase separation; membrane proteins; membrane fusion; virus-related materials

Special Issue Information

Dear Colleagues,

Living cell architecture is based on the concept of micro-compartmentation at different hierarchical levels. Cells themselves are self-bounded compartments, limited by a lipid membrane; eukaryotic cells have internal membrane-bound organelles dedicated to specific cellular functions, such as the cell nucleus, mitochondria and chloroplasts, the endoplasmic reticulum, the Golgi apparatus, as well as endosomes, lysosomes, etc. Moreover, membraneless compartments are currently under intense investigation in all types of cells. Compartments imply confinement and chemical gradients, and thus the non-homogeneous distribution of chemical species. Ultimately, compartmentation sustains fundamental processes for life maintenance, regulation, and information processing.

For decades, such complicated colloidal fine structures have attracted scientific attention. In addition to descriptive investigations, a bottom-up (constructive, synthetic) approach has recently emerged, often recognized within the bottom-up branch of Synthetic Biology.

Several biofunctions (in whole or in part) have been reconstituted in vesicles, usually—but not uniquely—made of lipids. Membraneless organelles have been recently featured thanks to experiments on liquid/liquid phase separation (LLPS) occurring in highly crowded solutions. Microdroplets made of hydrophilic polymer systems, similar to the PEG/dextran aqueous two-phase systems (ATPSs), are commonly used for modeling membraneless compartments. Various types of coacervates have shown complex cell-like behavior under several experimental conditions.

This Special Issue aims at collecting the most recent studies on artificial systems based on different types of compartmentalization. The final goal is the understanding of inter-cellular and intra-cellular mechanisms that contribute to the development of cellular complexity, revealing “emergent” properties occurring in cell and protocell systems. Biological meanings of interfaces and compartmentalization, set by not only membranous but also membraneless boundaries, will be discussed by viewing the results of theoretical consideration, wet experiments and plausible hypotheses based on artificial cell systems, such as membrane vesicles (liposomes), microemulsion droplets, and membraneless microdroplets emerging upon the micro-phase separation of the aqueous binary or multi-component (bio)polymer systems. These are considered to emerge as conventional and brand-new microstructures that assume intracellular environments highly crowded with biomacromolecules. The Special Issue also includes research presentations on related experimental/theoretical investigations; thus, let us think deeply about how (proto)cells could emerge as molecular microcompartment systems that developed their own interfaces.

We would like to elicit the submission of articles (full articles, reviews, etc.) related to the broad subject of membrane and membraneless microcompartments, their physico-chemical features, their use as cell or organellae models and, in general, about the peculiar characteristics of compartment architectures. All types of approaches are welcome (experimental, theoretical, conceptual, numerical simulations, etc.).

We look forward to receiving your best contributions and assembling a high-quality Special Issue.

Prof. Dr. Pasquale Stano
Prof. Dr. Kanta Tsumoto
Guest Editors

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Keywords

  • aqueous two-phase systems
  • artificial cells
  • coacervates
  • colloids
  • compartments
  • droplets
  • liposomes
  • liquid/liquid phase separation
  • membrane
  • membraneless
  • micelles
  • microdomains
  • organellae
  • proteinosomes
  • protocells
  • synthetic biology
  • synthetic cells
  • vesicles

Published Papers (6 papers)

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Editorial

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5 pages, 515 KiB  
Editorial
Membranous and Membraneless Interfaces—Origins of Artificial Cellular Complexity
by Pasquale Stano and Kanta Tsumoto
Life 2023, 13(7), 1594; https://doi.org/10.3390/life13071594 - 20 Jul 2023
Viewed by 792
Abstract
Living cell architecture is based on the concept of micro-compartmentation at different hierarchical levels [...] Full article
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Research

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11 pages, 3121 KiB  
Article
Evaporation Patterns of Dextran–Poly(Ethylene Glycol) Droplets with Changes in Wettability and Compatibility
by Chiho Watanabe and Miho Yanagisawa
Life 2022, 12(3), 373; https://doi.org/10.3390/life12030373 - 4 Mar 2022
Cited by 6 | Viewed by 2697
Abstract
The dextran–PEG system is one of the most famous systems exhibiting phase separation. Various phase behaviors, including the evaporation process of the dextran–PEG system, have been studied in order to understand the physicochemical mechanism of intracellular phase separation and the effect of condensation [...] Read more.
The dextran–PEG system is one of the most famous systems exhibiting phase separation. Various phase behaviors, including the evaporation process of the dextran–PEG system, have been studied in order to understand the physicochemical mechanism of intracellular phase separation and the effect of condensation on the origin of life. However, there have been few studies in dilute regime. In this study, we focused on such regimes and analyzed the pattern formation by evaporation. The specificity of this regime is the slow onset of phase separation due to low initial concentration, and the separated phases can have contrasting wettability to the substrate as evaporation progresses. When the polymer concentration is rather low (<5 wt%), the dextran–PEG droplets form a phase-separated pattern, consisting of PEG at the center and dextran ring of multiple strings pulling from the ring. This pattern formation is explained from the difference in wettability and compatibility between dextran and PEG upon condensation. At the initial dilute stage, the dextran-rich phase with higher wettability accumulates at the contact line of the droplet to form a ring pattern, and then forms multiple domains due to density fluctuation. The less wettable PEG phase recedes and pulls the dextran domains, causing them to deform into strings. Further condensation leads to phase separation, and the condensed PEG with improved wettability stops receding and prevents a formed circular pattern. These findings suggest that evaporation patterns of polymer blend droplets can be manipulated through changes in wettability and compatibility between polymers due to condensation, thus providing the basis to explore origins of life that are unique to the process of condensate formation from dilute systems. Full article
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11 pages, 2200 KiB  
Article
Colocalization Analysis of Lipo-Deoxyribozyme Consisting of DNA and Protic Catalysts in a Vesicle-Based Protocellular Membrane Investigated by Confocal Microscopy
by Yuiko Hirata, Muneyuki Matsuo, Kensuke Kurihara, Kentaro Suzuki, Shigenori Nonaka and Tadashi Sugawara
Life 2021, 11(12), 1364; https://doi.org/10.3390/life11121364 - 8 Dec 2021
Cited by 3 | Viewed by 2332
Abstract
The linkage between the self-reproduction of compartments and the replication of DNA in a compartment is a crucial requirement for cellular life. In our giant vesicle (GV)-based model protocell, this linkage is achieved through the action of a supramolecular catalyst composed of membrane-intruded [...] Read more.
The linkage between the self-reproduction of compartments and the replication of DNA in a compartment is a crucial requirement for cellular life. In our giant vesicle (GV)-based model protocell, this linkage is achieved through the action of a supramolecular catalyst composed of membrane-intruded DNA and amphiphilic acid catalysts (C@DNA) in a GV membrane. In this study, we examined colocalization analysis for the formation of the supramolecular catalyst using a confocal laser scanning fluorescence microscope with high sensitivity and resolution. Red fluorescence spots emitted from DNA tagged with Texas Red (Texas Red-DNA) were observed in a GV membrane stained with phospholipid tagged with BODIPY (BODIPY-HPC). To our knowledge, this is the first direct observation of DNA embedded in a GV-based model protocellular membrane containing cationic lipids. Colocalization analysis based on a histogram of frequencies of “normalized mean deviation product” revealed that the frequencies of positively correlated [lipophilic catalyst tagged with BODIPY (BODIPY-C) and Texas Red-DNA] were significantly higher than those of [BODIPY-HPC and Texas Red-DNA]. This result demonstrates the spontaneous formation of C@DNA in the GV membrane, which serves as a lipo-deoxyribozyme for producing membrane lipids from its precursor. Full article
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Review

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15 pages, 1589 KiB  
Review
Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions
by Naofumi Shimokawa and Tsutomu Hamada
Life 2023, 13(5), 1105; https://doi.org/10.3390/life13051105 - 28 Apr 2023
Cited by 3 | Viewed by 1752
Abstract
Lateral phase separation within lipid bilayer membranes has attracted considerable attention in the fields of biophysics and cell biology. Living cells organize laterally segregated compartments, such as raft domains in an ordered phase, and regulate their dynamic structures under isothermal conditions to promote [...] Read more.
Lateral phase separation within lipid bilayer membranes has attracted considerable attention in the fields of biophysics and cell biology. Living cells organize laterally segregated compartments, such as raft domains in an ordered phase, and regulate their dynamic structures under isothermal conditions to promote cellular functions. Model membrane systems with minimum components are powerful tools for investigating the basic phenomena of membrane phase separation. With the use of such model systems, several physicochemical characteristics of phase separation have been revealed. This review focuses on the isothermal triggering of membrane phase separation from a physical point of view. We consider the free energy of the membrane that describes lateral phase separation and explain the experimental results of model membranes to regulate domain formation under isothermal conditions. Three possible regulation factors are discussed: electrostatic interactions, chemical reactions and membrane tension. These findings may contribute to a better understanding of membrane lateral organization within living cells that function under isothermal conditions and could be useful for the development of artificial cell engineering. Full article
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25 pages, 6929 KiB  
Review
Evolution of Proliferative Model Protocells Highly Responsive to the Environment
by Muneyuki Matsuo, Taro Toyota, Kentaro Suzuki and Tadashi Sugawara
Life 2022, 12(10), 1635; https://doi.org/10.3390/life12101635 - 19 Oct 2022
Cited by 3 | Viewed by 2000
Abstract
In this review, we discuss various methods of reproducing life dynamics using a constructive approach. An increase in the structural complexity of a model protocell is accompanied by an increase in the stage of reproduction of a compartment (giant vesicle; GV) from simple [...] Read more.
In this review, we discuss various methods of reproducing life dynamics using a constructive approach. An increase in the structural complexity of a model protocell is accompanied by an increase in the stage of reproduction of a compartment (giant vesicle; GV) from simple reproduction to linked reproduction with the replication of information molecules (DNA), and eventually to recursive proliferation of a model protocell. An encounter between a plural protic catalyst (C) and DNA within a GV membrane containing a plural cationic lipid (V) spontaneously forms a supramolecular catalyst (C@DNA) that catalyzes the production of cationic membrane lipid V. The local formation of V causes budding deformation of the GV and equivolume divisions. The length of the DNA strand influences the frequency of proliferation, associated with the emergence of a primitive information flow that induces phenotypic plasticity in response to environmental conditions. A predominant protocell appears from the competitive proliferation of protocells containing DNA with different strand lengths, leading to an evolvable model protocell. Recently, peptides of amino acid thioesters have been used to construct peptide droplets through liquid–liquid phase separation. These droplets grew, owing to the supply of nutrients, and were divided repeatedly under a physical stimulus. This proposed chemical system demonstrates a new perspective of the origins of membraneless protocells, i.e., the “droplet world” hypothesis. Proliferative model protocells can be regarded as autonomous supramolecular machines. This concept of this review may open new horizons of “evolution” for intelligent supramolecular machines and robotics. Full article
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20 pages, 9680 KiB  
Review
Shape Deformation, Budding and Division of Giant Vesicles and Artificial Cells: A Review
by Ylenia Miele, Gábor Holló, István Lagzi and Federico Rossi
Life 2022, 12(6), 841; https://doi.org/10.3390/life12060841 - 6 Jun 2022
Cited by 11 | Viewed by 3337
Abstract
The understanding of the shape-change dynamics leading to the budding and division of artificial cells has gained much attention in the past few decades due to an increased interest in designing stimuli-responsive synthetic systems and minimal models of biological self-reproduction. In this respect, [...] Read more.
The understanding of the shape-change dynamics leading to the budding and division of artificial cells has gained much attention in the past few decades due to an increased interest in designing stimuli-responsive synthetic systems and minimal models of biological self-reproduction. In this respect, membranes and their composition play a fundamental role in many aspects related to the stability of the vesicles: permeability, elasticity, rigidity, tunability and response to external changes. In this review, we summarise recent experimental and theoretical work dealing with shape deformation and division of (giant) vesicles made of phospholipids and/or fatty acids membranes. Following a classic approach, we divide the strategies used to destabilise the membranes into two different types, physical (osmotic stress, temperature and light) and chemical (addition of amphiphiles, the addition of reactive molecules and pH changes) even though they often act in synergy when leading to a complete division process. Finally, we review the most important theoretical methods employed to describe the equilibrium shapes of giant vesicles and how they provide ways to explain and control the morphological changes leading from one equilibrium structure to another. Full article
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