Continuum elasticity and molecular dynamics of a pore in archaeal bolalipid membranes

Archaea are famous for their ability to survive in extremely harsh environments, probably due to the unprecedented stability of their lipid membranes. Key features of archaeal lipids (bolalipids) that confer their stability are methyl side groups and cyclopentanes in the alkyl chains, as well as the specific shape of the molecule, which has two headgroups connected by two tails. However, the contribution of each structural parameter to membrane stability and the underlying physical mechanism remain unknown. Here, we used molecular dynamics simulations to develop a method for measuring the energy of pore formation in bolalipid membranes as an assessment of their stability. In addition, we improved our previously developed continuum model by introducing a new term responsible for the rigidity of the alkyl chain. We calculated the pore edge energy and evaluated the membrane stability in terms of membrane elasticity. We demonstrated that increased stability of bolalipid membranes resulted both from hindered lateral mobility of these amphiphilic molecules and increased pore energy due to specific structure of bolalipids. Methyl side groups of bolalipids reduce the mobility of the molecules and increase the pore line tension in the same way as in the case of conventional phytanyl lipids. Chain rigidity hinders the formation of the bend molecules at the pore edge, thus additionally increasing the pore formation energy.