  Collagen type I is well-known for its outstanding mechanical properties which
it inherits from its hierarchical structure. Collagen type I fibrils may be
viewed as an heterogeneous material made of protein, macromolecules (such as
glycosaminoglycans and proteoglycans) and water. Water content modulates the
properties of these heterofibrils. Yet, the properties of water and the fine
interactions of water with the protein constituent of these nanocomposites have
only received limited attention. Here, we propose to model collagen type I
fibrils as an hydrated structure made of tropocollagen molecules assembled in a
microfibril crystal. We perform large-scale all-atom molecular dynamics
simulations of the hydration of collagen fibrils beyond the onset of
disassembly. We found that the structural and dynamic properties of water vary
strongly with the level of hydration of the microfibril. More importantly, we
found that the properties vary spatially within the 67 nm D-spacing periodic
structure. Alteration of the structural and dynamical properties of the
collagen microfibril occur first in the gap region. Overall, we identify that
the change in the role of water molecules from glue to lubricant between
tropocollagen molecules arises around 100% hydration while the microfibril
begins to disassemble beyond 130% water content. Our findings are supported by
a decrease in hydrogen bonding, recovery of bulk water properties and
amorphisation of the tropocollagen molecules packing. Our simulations reveal
the structure and dynamics of hydrated collagen fibrils with unprecedented
spatial resolution from physiological conditions to disassembly. Beyond the
process of self-assembly and the emergence of mechanical properties of collagen
type I fibrils, our results may also provide new insights in mineralization of
collagen fibrils.
