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Once Upon a Time the Cell Membranes: 175 Years of Cell Boundary Research Jonathan Lombard

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Once Upon a Time the Cell Membranes: 175 Years of Cell Boundary Research Jonathan Lombard Lombard Biology Direct (2014) 9:32 DOI 10.1186/s13062-014-0032-7 REVIEW Open Access Once upon a time the cell membranes: 175 years of cell boundary research Jonathan Lombard Abstract: All modern cells are bounded by cell membranes best described by the fluid mosaic model. This statement is so widely accepted by biologists that little attentionisgenerallygiventothe theoretical importance of cell membranes in describing the cell. This has not always been the case. When the Cell Theory was first formulated in the XIXth century, almost nothing was known about the cell membranes. It was not until well into the XXth century that the existence of the plasma membrane was broadly accepted and, even then, the fluid mosaic model did not prevail until the 1970s. How were the cell boundaries considered between the articulation of the Cell Theory around 1839 and the formulation of the fluid mosaic model that has described the cell membranes since 1972? In this review I will summarize the major historical discoveries and theories that tackled the existence and structure of membranes and I will analyze how these theories impacted the understanding of the cell. Apart from its purely historical relevance, this account can provide a starting point for considering the theoretical significance of membranes to the definition of the cell and could have implications for research on early life. Reviewers: This article was reviewed by Dr. Étienne Joly, Dr. Eugene V. Koonin and Dr. Armen Mulkidjanian. Keywords: Cell membrane discovery, Cell membrane structure, Cell Theory, History of Science, Cell definition, Origins of life, Early evolution, Cenancestor Introduction that maximizes both hydrophilic and hydrophobic interac- Modern descriptions of the cell are intimately related to tions [2]. These interactions may be affected by several pa- the notion of cell membranes. The cell membrane is not rameters, such as the chemical nature of the molecules, only the boundary of the unit of life, it is also a specific their size, the salinity and pH of the solution. In biological compartment that harbors many essential cell functions conditions, cell phospholipids form a bilayer in which including communication with the environment, transport hydrophobic tails face each other in the core of the of molecules and certain metabolic functions. Nowadays, structure whereas the hydrophilic heads interact with the consensual model to depict the membrane structure the surrounding water (Figure 1). Since proteins are and functions is called the “fluid mosaic model” [1]. also amphiphilic molecules, the same constraints apply The fluid mosaic hypothesis was formulated by Singer to them. Some proteins (called intrinsic or integral) are and Nicolson in the early 1970s [1]. According to this embedded in the lipid bilayer matrix where they are model, membranes are made up of lipids, proteins and able to establish hydrophobic and hydrophilic interactions carbohydrates (Figure 1). The main lipid membrane with their respective lipid counterparts. Other proteins, components are phospholipids. These molecules are called extrinsic or peripheral proteins, can also be amphiphilic, i. e. they have one polar part attracted by transiently associated with membrane surfaces through water (hydrophilic) and one apolar component repelled weaker interactions (Figure 1). Finally, carbohydrates by water (hydrophobic). When they are diluted in water, can be linked to either proteins or lipids, resulting in amphiphiles spontaneously adopt the most thermo- glycoproteins or glycolipids. dynamically stable molecular structure, namely the one The “mosaic” term of this model refers to the mixture of lipids and intrinsic proteins in the membrane. These boundaries are also “fluid” because their components Correspondence: [email protected] National Evolutionary Synthesis Center, 2024 W. Main Street Suite A200, can move laterally, allowing both diffusion of components Durham, NC 27705, USA © 2014 Lombard; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Lombard Biology Direct (2014) 9:32 Page 2 of 35 Figure 1 Fluid mosaic model. Schematic view of biological membrane structure as currently depicted. and local specific gatherings. Other lipids, such as choles- proteins. The presence of these molecules in the mem- terol, act as membrane fluidity regulators. Phospholipid branes doubles their bounding function with essential movements are generally restricted to lateral drift, because metabolic and bioenergetic activities. the cross of the membrane from one side to the other Except for some rare authors who still envisage the requires the energetically unfavorable transient contact of cell as a naked colloid network [4], there is nowadays lit- their hydrophilic head with the hydrophobic membrane tle disagreement that membranes are essential parts of core. Thus, the transfer of molecules from one side of the all contemporary cells. Despite this basic acceptance membrane to the other generally involves the activity of concerning modern cells, we have witnessed in recent some specific integral membrane proteins, called flippases years a strong debate questioning the presence of similar [3]. For the same reasons, integral proteins can diffuse membranes in the last common ancestor of living organ- within the lipid matrix but they seldom switch their polar- isms, namely the cenancestor. Arguing about the presence ity from one membrane side to the other. As a result, lipid, or absence of membranes in early organisms–not only the protein and carbohydrate composition are different be- cenancestor, but also previous organisms closer in time to tween the two monolayers, a characteristic that is referred the origins of life–challenges what we consider to be the to as membrane asymmetry. basic unit of life, i.e. the cell. Unfortunately, because the Membrane functions are extremely diverse. As cell lack of membranes is generally unquestioned in modern borders, membranes control the molecular exchanges organisms, it is nowadays difficult to come across discus- with the environment, resulting in cell pH regulation sions about the theoretical importance of membranes. and osmotic homeostasis. Membranes are “selective bar- The limited attention currently given to membranes in riers”: They concentrate nutrients within the cell, exclude defining the cell concept contrasts greatly with the im- the cellular waste products, keep the ionic gradients and portance that this issue had in early cell studies. Indeed, transform them into chemical energy. Since they allow the when the Cell Theory was formulated 175 years ago in the transduction of many external stimuli into cell signals, XIXth century, the reality of the membrane was unknown. they are also major actors in the responses of the cell to Its universal character was not generally acknowledged their environment. In addition, their composition also until well into the XXth century, and even when the cells turns membranes into the main apolar compartment of were assumed to be bounded by some kind of membrane, the prominently aqueous cell medium, thus concentrating the fluid mosaic model was not accepted until as late as most lipid pigments (e.g. chlorophyll) and hydrophobic the 1970s. The natural question then is: how were the cell Lombard Biology Direct (2014) 9:32 Page 3 of 35 boundaries envisioned between the formulation of the Cell The cell walls at the time of the cell theory proposal Theory around 1839 and the final predominance of the The construction of the cell concept was a complex fluid mosaic model in 1972? In this review, I will provide process that spanned the work of a large number of some answers to this question that I think will be useful in naturalists from the XVIIth to the XIXth centuries [11,12]. three different ways. First, it will considerably extend the Since it is not my intention here to discuss the history of range of some recent publications [5,6] in order to provide the Cell Theory, I will only deal with those authors whose a more complete account of the discovery of membranes work was particularly relevant for their conceptions of cell and their structure; Second, I will suggest that, contrary to membranes (see dark blue boxes in Figure 2). Because the ideas favored in some articles, the discovery of bio- many authors of this period wrote in German, the cita- logical membranes was not quite as a linear cumulative tions in the following sections will include both the pri- process as it has been generally depicted; And third, I mary and the secondary documents that I used to prepare expect that the acknowledgment of the importance of the this review. cell boundary concept on modern conceptions of the cell In 1665, Hooke observed a piece of cork with his will provide a fertile ground for discussions about the microscope and saw cavities that he compared to honey membranes in ancestral organisms. This, I hope, will open combs [13]. He named these cavities “cells”. This name new perspectives for the stimulating field of the origins of is revealing because from the start it suggests the exist- life. ence of some borders
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