Molecular bases of the adaptation to extreme environments (1 on 2)

Searching for the drivers of the adaptation to High Hydrostatic Pressure (HHP)

Why high hydrostatic pressure as an environmental driver ?

There is a large body of evidence which shows that life on Earth appeared as far as 3.8 billion years (Ga) ago. The catastrophic meteoritic bombardment ended between 4.2 and 3.9 Ga ago. Therefore, if life emerged, and we know it did, it must have emerged from nothingness in less than 400 million years. The most recent scenarios of Earth accretion predict some very unstable physico-chemical conditions at the surface of Earth, which, in such a short time period, would largely impede the emergence of life from a proto-biotic soup.

Some of the widely accepted scenarios suggest an origin for life in hydrothermal conditions in the depth of the Archaean ocean. The large body of water would have filtered the harmful radiation of the young sun  preventing their deleterious effects on the nascent organic matter, as well as buffered physico-chemical variations, providing a stable radiation-free environment for pre-biotic chemistry.

As a direct consequence, the first molecules, and the first cells, appearing onEarth would need to be adapted to high temperature and HHP. Today, the so-called deep-biosphere still represents most of the biotopes on Earth and is colonized by very specific organisms, adapted to multiple extreme conditions such as extreme oligotrophy, pH, temperatures, or hydrostatic pressure. If the routes to the adaptation to temperature are starting to be quite well understood, adaptive strategies of piezophilic organisms (requiring HHP for growth) which inhabit the deep-biosphere remain elusive.

The effect of high hydrostatic pressure on biological systems

The reason HHP affects biological systems because pressure affects chemical equilibria and reaction rates. The behavior of all systems under high pressure is governed by Le Châtelier's principle, which predicts that the equilibrium is shifted towards the state of smaller volume. Hence, a process is favored under HHP if its volume gets smaller with increasing pressure, and reversely it will be unfavored. Hence, in a cell, HHP has a different impact on depending on the biomolecules. When considering the main biomolecules, DNA, RNA, lipids and proteins, HHP will tend to stabilize the nucleic acids and lipids and destabilize the proteins. If one considers the functional components of the cell, such as replication, transcription, translation or metabolism, HHP will impair them, because it negatively impacts proteins. Similalry, HHP strongly impacts the cell membranes because upon compression, the lipids adapt to volume restriction by changing their conformation and packing (they essentially go from oil to butter). As a consequence, with increasing pressure the membrane loses in fluidity, becomes impermeable, and the protein-lipid interactions, which are essential to the optimal function of the membrane are weakened.

Life under pressure, the essence of being piezophile

In the deep-biosphere,HHP often exceeds that inhibitory to surface organisms. Microorganisms inhabiting these biotopes are able to grow more efficiently under HHP than under atmospheric pressure. These have been called piezophiles (from the greek piezo = to press and philo = love). In short, often inhibitory pressures for surface organisms are those optimal for piezophilic growth. Piezophilic organisms have been isolated from all high pressure environments (the deep-ocean, hydrothermal vents, the sub-seafloor or the continental underground). They belong to a wide variety of bacterial and archaeal genera. The most extreme piezophiles cannot survive at atmospheric pressure, and are called obligate piezophiles. The ability of piezophiles to grow under HHP inhibitory to surface organisms, and more so, the inability of the obligate piezophiles to grow at atmospheric pressure are proof that piezophiles have adapted to HHP in the course of their evolution.

In the scope of axis 1, the M2E team is asking a very simple and fundamental question : What are the structural and genetic bases between a surface organism and a piezophile which inhibits the growth of the former and stimulates the growth of the latter. This research has  been funded over the years by several national programs (ANR, CNRS MITI) and large instruments such as the ESRF (European Synchrotron Radiation Facility) or the Euroepan Neutron source of the ILL (Laue-Langevin Institute), which have supported our studies on the structural adaptation of the proteome in piezophiles or the on the structure of the membranes in pizophilic Archaea.

For more information on HHP adaptation in the piezophilic genome and proteome.

For more information on HHP adaptation in the membrane of piezophilic Archaea.