Chapter 8 – Theoretical Biophysics  329

where

t0 is some initial time

r is the position of an atom

u is the unitary vector for the pulling direction of the force probe

Uext can then be summed into the appropriate internal potential energy formulation used to

give a revised total potential energy function relevant to each individual atom.

The principal issue with SMD is a mismatch of time scales and force scales between simu­

lation outputs compared to actual experimental data. For example, single-​molecule pulling

experiments involve generating forces between zero and up to ~10–​100 pN over a time

scale of typically a second to observe a molecular unfolding event in a protein. However, the

equivalent time scale in SMD is more like ~10−9 s, extending as high as ~10−6 s in exceptional

cases. To stretch a molecule, a reasonable distance compared to its own length scale, for

example, ~10 nm, after ~1 ns of simulation implies a probe ramp speed equivalent to ~10 m

s−1 (or ~0.1 Å ps−1 in the units often used in SMD). However, in an experiment, ramp rates

are limited by viscous drag effects between the probe and the sample, so speeds equivalent

to ~10−6 m s−1 are more typical, seven or more orders of magnitude slower than in the SMD

simulations. As discussed in the section on reaction–​diffusion analysis later in this chapter,

this results in a significantly lower probability of molecular unfolding for the simulations,

making it nontrivial to interpret the simulated unfolding kinetics. However, they do still

provide valuable insight into the key mechanistic events of importance for force dependent

molecular processes and enable estimates to be made for the free energy differences between

different folded intermediate states of proteins as a function of pulling force, which provides

valuable biological insight.

A key feature of SMD is the importance of water-​solvent molecules. Bond rupture, for

example, with hydrogen bonds, in particular, is often mediated through the activities of water

molecules. The ways in which the presence of water molecules are simulated in general MD

are discussed as follows.

8.2.6  SIMULATING THE EFFECTS OF WATER MOLECULES AND SOLVATED IONS

The primary challenge of simulating the effects of water molecules on a biomolecule

structure is computational. Molecular simulations that include an explicit solvent take

into account the interactions of all individual water molecules with the biomolecule. In

other words, the atoms of each individual water molecule are included in the MD simu­

lation at a realistic density, which can similarly be applied to any solvated ions in the

solution. This generates the most accuracy from any simulation, but the computational

expense can be significant (the equivalent molarity of water is higher than you might

imagine; see Worked Case Example 8.1).

The potential energy used is typically Lennard–​Jones (which normally is only applied to

the oxygen atom of the water molecule interacting with the biomolecule) with the addition

of the Coulomb potential. Broadly, there are two explicit solvent models: the fixed charge

explicit solvent model and the polarizable explicit solvent model. The latter characterizes

the ability of water molecules to become electrically polarized by the nearby presence of the

biomolecule and is the most accurate physical description but computationally most costly.

An added complication is that there are >40 different water models used by different research

groups that can account for the electrostatic properties of water (e.g., see Guillot, 2002),

which include different bond angles and lengths between the oxygen and hydrogen atoms,

different dielectric permittivity values, enthalpic and electric polarizability properties, and

different assumptions about the number of interaction sites between the biomolecule and the

water’s oxygen atom through its lone pair electrons. However, the most common methods

include single point charge (SPC), TIP3P, and TIP4P models that account for most biophys­

ical properties of water reasonably well.