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 J.R.C. van der Maarel
INTRODUCTION TO INTRODUCTION TO
BIOPOLYMER
BIOPOLYMER

INTRODUCTION TO BIOPOLYMER PHYSICS

Johan R. C. van der Maarel

PHYSICS
T
his book provides an ideal introduction to
the physics of biopolymers. The structure,
dynamics, and properties of biopolymers
subjected to various forms of confinement are
PHYSICS
covered, and special attention is paid to the
effect of charge and electrostatic screening
(polyelectrolyte effect). By focusing on the
development of physical intuition rather than
mathematical rigor, readers will be better
prepared to address complicated, real issues
in the life sciences or related fields such as
material or food sciences. The book is designed
to serve as a bridge between undergraduate
textbooks in physical (bio)chemistry and the
professional literature, and is thus especially
suitable for advanced undergraduate or
postgraduate students and professionals
who have already acquired basic knowledge
of physics, thermodynamics, and molecular
biology.

ISBN-13 978-981-277-603-7
ISBN-10 981-277-603-6
World Scientific
www.worldscientific.com ,!7IJ8B2-hhgadh! World Scientific
6644 hc
Copyright by Johan R. C. van der Maarel

All rights reserved

TO MY CELESTIAL DANCERS

ANNE AND LIEVE

AND TO

PASCALE

FOR HER FORBEARANCE

 vii

PREFACE

This book is an introduction to the physics of biopolymers. After a brief

overview of the basic properties, we will focus on the structure and dynamics
of biopolymers subjected to various forms of confinement. Examples are
biopolymers in nano-channels, exposed to external forces, grafted at an
interface to form a brush or under crowded conditions at high concentrations
in the semi-dilute regime. Special attention will be paid to the effect of charge
and electrostatic screening (polyelectrolyte effect). Along the way, we will also
discuss higher order secondary and tertiary structures and their transitions.
Finally, we will consider the properties of biopolymers in congested and
crowded states, which bear resemblance to the situation in living cells and
organisms.
The book is primarily aimed at the development of physical intuition
rather than mathematical rigor in order to prepare the reader to address
complicated, real issues in the life sciences or other related fields such as
material or food sciences. Most, if not all of the material has been treated with
the simplest approach, without losing scientific significance. The mathematics
is not too complicated and can be handled by anyone who has received a basic
training in calculus. The book is intended to serve as a bridge between
undergraduate textbooks in the area of physical (bio) chemistry and
professional literature. Accordingly, it is targeted at the advanced
undergraduate or postgraduate student as well as the professional, who has
already acquired a basic knowledge of physics, thermodynamics and molecular
biology.
The book is based on my lecture notes for a course on biopolymer physics
for fourth year students, which I teach at my home institution. Surely, the
quantity of the material exceeds the amount which can be taught in a single
viii

term and the lecturer might want to make a selection. For instance, one can
drop the section on polyelectrolyte brushes or one can skip one of the more
specialized topics, such as the compaction of the genome in the capsid of
bacteriophages. I plan to post the answers to the questions, small computer
script files and other relevant updates (including corrections) on my research
group’s website: http://www.physics.nus.edu.sg/~bcf/.
It is a pleasure to thank all those people who have contributed, either
directly or indirectly, to the writing of this book. First, there are my former
teachers and colleagues who have diligently explained to me the older and
therefore perhaps less known literature on polymers and polyelectrolyes.
Then, of course, I owe thanks to my former and present students. They have
pointed out many mistakes in my lecture notes on which this book is based
and they have forced me to explain the material in as transparent a way as
possible. Special thanks are due to Claire Lesieur for informing me about the
status of our understanding of protein folding. I thank Rudi Podgornik for
enlightening discussions about the Poisson–Boltzmann equation for
polyelectrolytes in the presence of salt. Furthermore, I am grateful to Daniel
Blackwood for proof-reading the manuscript. It goes without saying that the
responsibility for any possible remaining errors and/or inconsistencies lies
entirely with the author. Finally, I thank Pascale, Anne and Lieve for their
patience and I apologize for the many hours I took from our precious family
time.

Singapore, July 2007.

 ix

CONTENTS

CHAPTER 1 BIOPOLYMERS 1
1.1 Introduction 1
1.2 Primary structures 4
1.2.1 Nucleic acid primary structures 4
1.2.2 Protein primary structures 6
1.2.3 Polysaccharide primary structures 9
1.3 Secondary structures 11
1.3.1 Secondary structures of nucleic acids 11
1.3.2 Secondary structures of proteins 14
1.3.3 Secondary structures of polysaccharides 17
1.4 Tertiary structure and stabilizing interactions 17
1.5 Questions 20

CHAPTER 2 POLYMER CONFORMATION 23

2.1 The ideal chain 23
2.2 The Kuhn chain 26
2.3 The worm-like chain 27
2.4 Excluded volume interactions 32
2.5 Confinement in a tube; introduction to scaling 34
2.6 Deflection in a narrow tube 36
2.7 Stars and radial brushes 38
2.8 Chains under traction 39
2.8.1 An ideal chain under small tension 40
2.8.2 Worm-like chain 40
2.8.3 Swollen chain 42
2.9 From the dilute to the semi-dilute regime 45
2.10 Chain statistics in the semi-dilute regime 49
2.11 Questions 51
x

CHAPTER 3 POLYELECTROLYTES 55
3.1 Counterion condensation 55
3.2 The electrostatic potential 61
3.3 The non-linear Poisson–Boltzmann equation 66
3.3.1 Polyelectrolytes in excess salt 66
3.3.2 Charge distribution in the cell model 69
3.4 The electrostatic persistence length 76
3.5 Electrostatic excluded volume 80
3.6 Flexible chains and electrostatic blobs 87
3.7 Spherical polyelectrolyte brushes 89
3.7.1 Spherical polyelectrolyte brush without salt 89
3.7.2 Salted spherical polyelectrolyte brush 94
3.8 Polyelectrolytes in the semi-dilute regime 99
3.8.1 Salt-free polyelectrolytes; a hierarchy of blobs 99
3.8.2 Salted polyelectrolytes 101
3.9 Questions 103

CHAPTER 4 POLYMER DYNAMICS 105

4.1 Single chain dynamics 105
4.2 Pulling a chain into a hole 111
4.3 Dynamics of non-entangled chains in the semi-dilute regime 114
4.4 Entangled polymer dynamics; reptation 117
4.5 Dynamic scaling of polyelectrolytes 121
4.5.1 Polyelectrolytes without salt 121
4.5.2 Salted polyelectrolytes 124
4.5.3 Comparison with experimental results 126
4.6 Gel electrophoresis 130
4.7 Questions 134

CHAPTER 5 HIGHER ORDER STRUCTURES AND THEIR TRANSITIONS 137

5.1 Supercoiled DNA 137
5.1.1 Topology 138
5.1.2 Molecular free energy 142
5.1.3 Long-range structure and branching 151
5.2 Alternate secondary DNA structures 155
5.2.1 B–Z transition 155
5.2.2 Cruciforms 159
5.3 Helix-coil transition 161
5.4 Protein folding 167
5.5 Questions 171
 xi

CHAPTER 6 MESOSCOPIC STRUCTURES 175

6.1 Lyotropic liquid crystals 175
6.1.1 Virial theory 177
6.1.2 Liquid crystalline orientation order 182
6.1.3 Isotropic-anisotropic phase coexistence 185
6.2 Hexagonal packing of DNA 190
6.2.1 Undulation enhanced electrostatic interaction 191
6.2.1 Melting of the hexagonal phase 196
6.2.2 DNA equation of state 198
6.3 Bacteriophage DNA packaging 201
6.4 Crowding and entropy driven interactions (depletion) 208
6.4.1 Entropic colloidal interactions in solutions of macromolecules 210
6.4.2 Phase separation of small particles in a polymer solution 215
6.5 Questions 220

APPENDIX A: POISSON–BOLTZMANN THEORY FOR A MONOVALENT SALT 223

APPENDIX B: SUMMARY OF SCALING LAWS 227

APPENDIX C: LIST OF IMPORTANT SYMBOLS 229

RECOMMENDED READING 233

REFERENCES 235

INDEX 243
 Introduction to Biopolymer Physics 1

CHAPTER 1

BIOPOLYMERS

In this chapter, the basic properties of biopolymers will be briefly discussed.

We will group them according to nucleic acids, proteins and polysaccharides
and we will summarize their main biological functions. Biopolymers have the
unique feature that they exhibit a hierarchy in their molecular structures.
Associated with these structures, their biological functions emerge almost
naturally. In the latter context, think about the importance of the double-
helical structure of DNA for the replication process. It is important to realize
that these biological functions are based on the way the building blocks
(nucleotides, amino acids, carbohydrates, etc.) are assembled. We will
subsequently present the primary, secondary and some tertiary structures of
nucleic acids, proteins and polysaccharides and show how they are stabilized
by interactions. However, a detailed discussion of the chemical composition
of the various biopolymers and their biological functions is beyond the scope
of this book and for this purpose the reader is referred to the dedicated
literature (see, for instance, the textbooks of Mathews, van Holde and Ahern
and Bloomfield, Crothers and Tinoco).1,2

1.1 Introduction

Biopolymers or biomacromolecules can be roughly classified according to

three different categories: nucleic acids, proteins and polysaccharides
(carbohydrates). It should be born in mind that this classification is not strict
and that there are important exceptions. An example is glycoprotein, which is
a combination of protein and carbohydrate and plays a role in, among others,
immune cell recognition and tissue adhesion. The biological functions of
nucleic acids, proteins and polysaccharides are also different. Nucleic acids are
2 Chapter I: Biopolymers

involved with the storage of the genetic code (DNA) and the translation of
the genetic information into protein products (RNA). Proteins catalyze
biochemical reactions (enzymes), have structural or mechanical functions or
are important in cell signalling and immune responses. The structural
components of plants are primarily composed of the polysaccharide cellulose.
Bacteria excrete polysaccharides for adhesion to surfaces and to avoid
dehydration. Examples of these polysaccharides are dextran, xanthan and
pullulan, which have found wide-spread applications in pharmacy,
biotechnology and the food industry. The classification according to the
functioning of the biopolymers is also not unique. An important exception is
the ribosome; an organelle on which proteins are assembled. A ribosome
contains 65% RNA and 35% protein. It can be considered an enzyme, but its
active site is made of RNA. However, the functioning and purpose of
biopolymers in the machinery of life is beyond the scope of this book. Here,
we intend to explore the extent to which their properties can be understood in
terms of concepts from physics and mathematics.
Like every polymer, biopolymers are strings or sequences of monomeric
units or monomers for short. In many cases these strings are linear, but
sometimes they are closed and circular, branched or even cross-linked. In the
latter case, we are dealing with a gel. In this book, we will primarily focus on
linear polymers, but we will also discuss star-branched polymers, spherical
polymer brushes and closed circular, supercoiled DNA. The structure of any
biopolymer is determined by the nature of the building blocks (i.e. the
monomeric units) in combination with environmental conditions such as the
temperature, the solvent (water) and the presence of salts and/or other
molecular components. The monomeric units of nucleic acids, proteins and
polysaccharides are largely different and will be discussed in the next section.
A unique feature of biopolymers is that most of them are essentially
heteropolymers, because they may contain a variety in monomeric units. The
biological relevance of a biopolymer is ultimately based on the sequence of the
monomers, i.e. the primary structure. In the case of DNA, the primary
structure is the sequence of bases attached to the sugar rings, which
determines the genetic code. For proteins, it is the amino acid sequence, which
eventually determines, together with environmental conditions, their 3–
dimensional shapes and biological functions. The properties of
polysaccharides are also largely determined by the nature of the monomeric
 Introduction to Biopolymer Physics 3

units, more specifically in the way they are connected.

A fundamental characteristic of biopolymers is the formation of
hierarchical structures at successive length scales. Starting from the primary
structure, the monomeric units are organized in a certain local molecular
conformation. This local conformation is commonly referred to as the
secondary structure. Examples of secondary structures are the famous double-
helical arrangement of the two opposing strands in the DNA molecule (the
duplex) and α − helixes and β − sheets formed by the polypeptide chains in
proteins. At a larger distance scale, a biopolymer can adopt a defined 3–
dimensional conformation: the so-called tertiary structure. This is particularly
relevant for proteins, which largely owe their biological functioning to their
3–dimensional structure, but also nucleic acids and polysaccharides have
tertiary structures. An example of a nucleic acid with a tertiary structure is
transfer RNA, which has an L–shaped 3–dimensional structure that allows
them to fit into the active site of the ribosome (it transfers a specific amino
acid residue to a growing polypeptide chain). Eventually, biopolymers can
form even larger complexes among themselves and with other macromolecular
components in the cell and organism.
Biopolymers have emergent properties associated with their hierarchical
structures. Here, the meaning of emergence is that the biopolymers have
properties that cannot be attributed to the individual building blocks. For
instance, the nucleic acid bases are just molecular components made of
carbon, nitrogen and oxygen. It is their specific sequence in a strand of the
DNA or RNA molecule that carries the genetic code. This property cannot be
attributed to the individual bases, but it has emerged from the assembling of
the bases into the nucleic acid. It is also obvious that the activity of a protein is
an emerging property of the hierarchical assembling of the amino acids. Here,
it is even possible to replace a selected and limited number of amino acids by
other amino acids without losing the biological function of the protein.
Emergence is a general phenomenon associated with the assembling of
building blocks into larger scale structures, both in civil engineering and in
biology.
Throughout this book, we will almost exclusively deal with systems in
thermodynamic equilibrium. Although this is of interest in its own right, it is
only fair to say that the study of systems in thermodynamic equilibrium has a
limited relevance for our understanding of life. It is commonly believed that
4 Chapter I: Biopolymers

O 5’ end O 5’ end
O P O O P O

O O
5’ CH2 Base 5’ CH2 Base
O O

3’ 3’
O OH O
O P O O P O

O O
5’ CH2 Base 5’ CH2 Base
O O

3’ 3’
3’ end O OH 3’ end O

RNA DNA

Figure 1.1 Chemical structures of ribonucleic acid (RNA, left) and deoxyribo-
nucleic acid (DNA, right). The phosphate groups and the five carbon sugar
rings are shown in detail. The bases are shown schematically, but their
chemical structures are depicted in Fig. 1.2.

spontaneous assembling processes, driven by the minimization of the system’s

free energy (self-assembly), are important in biology. However, one should
bear in mind that life exists by the virtue of the dissipation of energy, mainly
through the hydrolysis of adenosine triphosphate (ATP). By definition, a
living organism is in a non-equilibrium state and it is not always possible to
generalize the concepts obtained for equilibrium conditions. Understanding
life on the basis of non-equilibrium, dissipative processes is clearly a challenge
for the future.

1.2 Primary structures

1.2.1 Nucleic acid primary structure

There are two types of nucleic acids, ribonucleic acid (RNA) and
deoxyribonucleic acid (DNA). As shown in Fig. 1.1, each molecule is a
 Introduction to Biopolymer Physics 5

NH 2 NH2
Adenine (A) N Cytosine (C)
N N
DNA/RNA DNA/RNA
N N O N O
Sugar Sugar
Uracil (U) HN
RNA
O N
O O
Sugar
Guanine (G) N Thymine (T) HN
NH
DNA/RNA DNA
N N NH2 O N
Sugar Sugar

Figure 1.2 Pyrimidine (cytosine, C; thymine, T; uracil, U) and purine (adenine,

A; guanine, G) bases in DNA and RNA.

polymeric chain, in which the units are covalently linked by the phosphates.
The monomeric units are the nucleotides. Each nucleotide is built around a
five-carbon sugar; ribose in RNA and 2’–deoxyribose in DNA. In Fig. 1.1 the
five carbon atoms of the sugar are counted from the one to which the base is
attached at the right, down through the ring and then up to the fifth carbon at
the upper left side. Besides a difference in bases, which will be discussed
shortly, the chemical difference between RNA and DNA lies in the
replacement of a hydroxyl group by a hydrogen atom at the 2’ position in
DNA. The nucleotides are linked through the formation of a phosphodiester
between the 5’ carbon of one nucleotide and the 3’ carbon of the next
nucleotide. In this way, long nucleic acid chains sometimes contain millions of
units which are attached to each other. It is important to realize that the string
of nucleotides has a direction from the 3’ to the 5’ end. The phosphate group
is a strong acid with a pK a of around one. RNA and DNA are thus strong
acids and under physiological conditions every phosphate moiety carries a
negative charge. DNA and RNA are so-called polyelectrolytes and the
presence of charge results in specific properties, such as an electrostatic
contribution to the bending rigidity of the molecule. This and other effects of
the presence of charge will be detailed in Chapter 3.
The backbone of the nucleic acid molecule is a repetitive structure and by
itself it cannot store information. It is clear that the information storage
6 Chapter I: Biopolymers

capacity is derived from the sequence of bases, each of which is attached to the
1’ carbon of the sugar ring. There are two types of bases: the purines and
pyrimidines. In the case of DNA, there are two purines, adenine (A) and
guanine (G) and two pyrimidines, cytosine (C) and thymine (T). In the case
of RNA, uracil (U) replaces thymine (see Fig. 1.2). DNA and RNA also
contain a small fraction of chemically modified bases; some of these can
induce alternate secondary structures, as will be discussed in Chapter 5. Note
that the bases do not carry charge, but they can form hydrogen bonds.

1.2.2 Protein primary structure

All proteins are polymers and their monomeric units are α − amino acids.
The amino group is attached to the α − carbon, i.e. the carbon next to the
carboxyl group. Under physiological conditions, the amino acid is in its
zwitterionic form; the amino group has picked up a proton and has become
positively charged and the carboxyl group has dissociated a proton and is
negatively charged. Besides the amino group, a hydrogen atom and a side
group are also attached to the α − carbon of every amino acid. The amino
acids are distinguished by their different side groups. Twenty chemically
different amino acids are incorporated in proteins; their structures are shown
in Fig. 1.3. In the simplest case, glycine, the side group is just a hydrogen atom.
The amino acids can be grouped according to the physical-chemical properties
of the side group: aliphatic, hydroxyl or sulphur containing, cyclic (proline),
aromatic, basic or acidic. It is clear that the higher order secondary and tertiary
structures of proteins are intimately related to these properties, together with
environmental factors such as the solvent quality.
With the exception of glycine, there are always four different chemical
groups attached to the α − carbon of every amino acid. Accordingly, amino
acids are chiral and each one can occur in two different stereoisomers: the D–
and L–forms. The L–form of alanine is displayed in Fig. 1.4; it has the amino,
hydrogen, carboxyl and methyl groups arranged in a clockwise manner, when
the α − carbon is viewed from the top with the amino and carboxyl groups
pointing downwards and the hydrogen and methyl group pointing upwards.
All amino acids incorporated by organisms into proteins are of the L–form.
The chirality of the amino acids has an important consequence for the
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