Give an example of an organism and its adaptation to an extreme environmental condition (for example, extreme cold, heat, low water or nutrient availability, disturbance to its habitat). For full credit, describe how the adaptation allows the organism to survive in those conditions.
Extremophilic organisms are primarily
prokaryotic (archaea and bacteria), with few
eukaryotic examples. Extremophiles are defined by the environmental
conditions in which they grow optimally. The organisms may be
described as acidophilic (optimal growth between pH 1 and pH 5);
alkaliphilic (optimal growth above pH 9); halophilic (optimal
growth in environments with high concentrations of salt);
thermophilic (optimal growth between 60 and 80 °C);
hyperthermophilic (optimal growth above 80 °C); psychrophilic
(optimal growth at 15 °C or lower, with a maximum tolerant
temperature of 20 °C and minimal growth at or below 0 °C);
piezophilic, or barophilic (optimal growth at high hydrostatic
pressure); oligotrophic (growth in nutritionally limited
environments); endolithic (growth within rock or within pores of
mineral grains); and xerophilic (growth in dry conditions, with low
water availability). Some extremophiles are adapted simultaneously
to multiple stresses (polyextremophile); common examples include
thermoacidophiles and haloalkaliphiles. Extremophiles are of
biotechnological interest, as they produce extremozymes, defined as
enzymes that are functional under extreme conditions. Extremozymes
are useful in industrial production procedures and research
applications because of their ability to remain active under the
severe conditions typically employed in these processes. The study
of extremophiles provides an understanding of the physicochemical
parameters defining life on Earth and may provide insight into how
life on Earth originated. The postulations that extreme
environmental conditions existed on primitive Earth and that life
arose in hot environments have led to the theory that extremophiles
are vestiges of primordial organisms and thus are models of ancient
life.
Volcanic hydrothermal springs possess an astonishing diversity of
organisms at the base of oasis of life in the abyss (Black smokers’
ecosystems). Hypersaline environments such as large salt lakes or
the Dead Sea are also populated by microorganisms that only develop
when the salt concentration becomes intolerable for any other form
of life. Glacial and polar environments also support rich
populations of microbes. Finally, there are significant microbial
communities on the ocean floor, in sediments and deep geological
layers. It is estimated that 80% of terrestrial ecosystems are
permanently exposed to temperatures below 5°C, often under high
pressure conditions. Thus, on a global scale, extremophiles can no
longer be considered as exceptions.
Little is known about the roles of extremophiles in ecosystems,
including climate regulation. Recent work shows that their
contribution to the production of greenhouse gases, and to the
major carbon, nitrogen and nitrate cycles, is far from negligible.
Often, their genome contains more than 90% of genes encoding
proteins with unknown functions. For what reasons? Biological
macromolecules must necessarily adapt to the physico-chemical
conditions, nutritional and energy resources specific to these
extreme environments. These constraints may lead to the emergence
of new metabolic pathways using different substrates and co-factors
than those used by “conventional” organisms.
The discovery of the Archaea: a revolution
Many extremophilic organisms are archaea, a group of microbes that have molecular characteristics that clearly distinguish them from the other two forms of life well known to the public: bacteria and eukaryotes . This third life form was first proposed by the American biologist Karl Woese in 1990. Using ribosome RNA as a molecular tracer, Woese sought to reconstruct the universal tree of the evolution of life. Since then, the identification of a growing number of new archaea species and the study of their genomes has shown that this is indeed a reality. As single-cell organisms without nuclei, such as bacteria (Figure 3), archaea have remarkable properties. They have their own viruses. Even more surprisingly, some archaea are capable of symbioses with complex organisms such as sponges. Archaea are found in the gut microbiota, which plays an important role in humun. No pathogens have yet been identified in archaea, but their link to certain diseases or metabolic disorders such as obesity has been proven. The evolution and expansion of archaea and bacteria are equally complex. Archaea have an astonishing evolutionary proximity to eukaryotes. Some hypotheses suggest that archaea are at the origin of the emergence of eukaryotes.
Hyperthermophilic archaea: Thermococcus fumicolans.Archaea seem particularly suitable for development under the most extreme conditions known on Earth. For this reason, they were initially considered to be poorly diversified and only associated with volcanic hot springs and hypersaline lakes. This initial vision was totally biased. Molecular ecology studies have revealed very many archaean lines in all terrestrial environments. Indeed, we are discovering more and more “non-extremophilic” archaea that would represent 25% of microbial life in oceans and soils. They should therefore no longer be considered as marginal, archaic or primitive forms of life. In addition, their extremophile character allows them to be better activated or inhibited. For these reasons, and thanks to the recent development of genetic tools, archaea represent excellent models for integrative biology combining in vivo studies, biochemistry, biophysics and structural biology. These studies were the first to determine the structure of many cellular machinery and are the source of many drugs such as anti-cancer drugs.
Extremophilic organisms and the limits of life
To develop, life needs:
• carbon, the basic element of biological
macromolecules;
• water, the most conducive solvent for the functioning
of proteins;
• energy, necessary for the functioning of biological
systems.
Energy is provided by light, by electron-donating elements such as
metals and finally by the breaking of chemical bonds catalyzed by
enzymes. The discovery of microbial communities in environments
long considered sterile has shown that the physico-chemical limits
within which life can develop are much more extensive than
previously thought. These organisms, which are grouped under the
name of extremophiles, are not in “survival” conditions but really
need conditions considered hostile in order to develop.
In hydrothermal springs (Black smokers’ ecosystems), archaea and
bacteria called “thermophilic” or “hyperthermophilic” only develop
optimally at high temperatures, sometimes above 110°C. Some,
isolated in the abyss such as the Marianas pit, are piezophiles:
they need pressures exceeding 20 MPa. In the seabed, lakes and
glacial environments, “psychophiles” only thrive below 15°C and
down to -12°C . In hypersaline environments, open water is rare
because it is largely trapped by saline ions. The result: cells are
destroyed and proteins are denatured. Nevertheless, so-called
“halophilic” organisms have a particular biochemistry that
preserves their cellular integrity under conditions of severe
dehydration. Ecosystems associated with hydrothermal springs,
geological effluents or hyper-saline environments often have
extreme pH conditions (0 and 13). Thus, most of the organisms that
live there are poly-extremophiles.
In addition to extreme and often highly fluctuating
physico-chemical conditions, extremophiles are also confronted with
multiple environmental stresses such as radiation or heavy metals.
These agents generate free radicals that damage DNA and proteins.
Most extremophilic microbes have developed DNA repair systems and
protein recycling systems that enable them to resist radiation
doses of up to 10,000 Gray. The exploitation of the environment’s
energy resources is another frontier of life that the study of
extreme microbes leads us to constantly push back. Thus,
extremophiles seem particularly adapted to stresses resulting from
very low energy and/or nutrient flows. Thus, some live and develop
very slowly in the deep sediments of the oceans or several
kilometres inside the Earth’s mantle.
Ganymede is the largest moon in our solar system and the only moon with its own magnetic field. According to NASA, there is a salty ocean 100 km deep under a layer of ice [Source: Felicia Chou, NASA].The discovery and study of archaea, more globally of extremophilic microbes, has changed our conceptions on the habitability of the Earth. They guide our ideas in the search for possible traces of life on other planets . For example, microbes capable of surviving arid and cold conditions have been discovered in the Atacama Desert in Chile. Halophilic organisms are capable of developing at -15°C. Other microbes are strictly associated with high pressures, which are interesting observations to consider after the discovery of liquid brines on Mars, deep oceans and hydrothermal activities on moons of Saturn and Jupiter such as Europe and Ganymede.
How do extremophiles preserve their biological
functions?
The maintenance of stable and functional biological membranes is a
first condition for allowing cellular life in extreme conditions of
temperature, pressure or salinity. Membranes are essential to
produce energy and compartmentalize biochemical activities. Changes
in the composition of membrane lipids allow them to adapt to high
and low temperatures and very high pressures that affect the
fluidity of membranes.
In non-extremophilic organisms, exposure to “extreme”
physico-chemical conditions inactive or even denatures certain
proteins. Extremophilic adaptation also consists in preserving the
assembly of cellular machines and the three-dimensional folding of
the polypeptide chains that constitute proteins. This folding is
responsible for the biochemical activity of enzymes. Understanding
the mechanisms that stabilize biological macromolecules under
extreme conditions is not only useful for understanding:
(i) the origins and expansion capacities of living
organisms,
(ii) the fundamental processes that govern the functioning of
proteins and
(iii) the universal cellular processes designed to maintain the
integrity of cellular machinery.
A first strategy widely used by extremophiles to preserve their
cellular constituents is to synthesize and accumulate small
molecules (trehalose, betaines, etc.) in the cytoplasm that
stabilize molecular structures. Maintaining protein integrity and
homeostasis also involves optimizing chaperone and protein
modification systems to prevent aggregation, assist folding or
trigger rapid destruction by intracellular proteases. These protein
“quality control” systems are crucial both for the adaptation of
thermophilic organisms and for psychophiles. They are not specific
to extremophiles but are preserved in all living beings, including
humans. Thus, systems derived from extremophilic microorganisms are
simple models for understanding the fundamental mechanisms of
stress response, degenerative diseases and aging processes.
The cellular mechanisms that preserve the integrity of biological
macromolecules require a lot of energy from the cells. This is why
the proteins of true extremophiles have highly modified properties.
Acquired during evolution via mutations, these modifications
stabilize proteins under conditions of high temperature, salt or
pressure. However, the comparison of crystallographic structures of
proteins from extremophilic organisms with their mesophilic
counterparts shows little difference in the overall architecture of
the structures. On the other hand, the selected mutations generate
very different biophysical properties. For example, thermophilic
proteins are “frozen” at room temperature. The cause: a stiffening
of the macromolecular structure due to the optimization of
intramolecular interactions. This gives proteins extraordinary
strength. However, while maintaining the three-dimensional
structure is essential for the functioning of biological
macromolecules, proteins also have overall dynamic properties. Some
regions must move to recognize substrates, co-factors and perform
complex biochemical functions.
The constraints on molecular structures by different
environmental parameters are not the same, resulting in different
adaptive strategies. Thus, for thermophiles, the main challenge is
to prevent protein folding. Adaptation consists in strengthening
the forces that stabilize protein folding while maintaining
significant flexibility in regions dedicated to the biochemical
functioning of enzymes. The main consequence of low temperatures is
to slow down the speed of chemical reactions. In psychrophilic
proteins, adaptation is rather due to a modification of the active
sites allowing a better catalytic efficiency, associated with a
global or local relaxation of intramolecular constraints within
them. These modifications maintain a slow but sufficient metabolism
to allow cell division. By reducing the amount of free water and
interacting with polypeptide chains, salt affects protein
solubility and disrupts the intramolecular interfaces that cause
folding. However, halophilic proteins have accumulated mutations
that allow them to counteract these effects and even interact
advantageously with solvent ions. These associations both
contribute to stabilizing the structure while maintaining a layer
of hydration necessary for the system to operate. Adaptation is so
advanced here that most of the proteins from these organisms are
only soluble and folded under hypersaline conditions. Finally,
recent research reveals molecular adaptation associated with high
hydrostatic pressure conditions in the abysses and deep geological
layers of the planet. In this case, the cavities present within
molecular structures that are mostly modified.
In all types of adaptations associated with life in “extreme”
conditions, changes in protein structures profoundly alter the
biochemistry and physiology of biological systems. For this reason,
conditions that we consider “normal”: temperatures of 37°C,
salinity of 3%, atmospheric pressure, presence of oxygen, etc. are
in fact hostile conditions for most extremophiles. These conditions
cause stress to the cells. For example, water is a deadly solvent
for halophiles . These organisms accumulate almost saturated
concentrations of salt in their cytoplasm, ensuring the solubility
and correct folding of their proteins. On a geological scale,
climatic variations of great amplitude have established extreme
conditions on the surface of the planet. It is also for this reason
that the notion of extremophilia must be put into perspective.
Usefulness of “extremozymes” for
biotechnologies
Enzymes are natural products that perform chemical reactions in an
ultra-efficient and non-polluting way. In a context of food and
environmental crisis requiring the development of a bio-inspired
economy, the new enzymes found in the genomes of populations of
extremophilic microorganisms (and called extremozymes) are of great
interest. Indeed, their robustness, their ability to perform
chemical reactions under extreme conditions and sometimes the
uniqueness of the chemical reactions they perform make them very
interesting for multiple applications. For example, biotechnologies
use extremozymes for the production of biofuels, bio-materials or
pharmaceutical molecules. Halophilic enzymes are capable of
operating in saline environments, in organic solvents and in a wide
range of pH. They are used in food processing, in the paper
industry as well as in the textile industry.Thermozymes and
barozymes from thermophilic and/or barophilic organisms are
hyperstable enzymes that can be used for food applications under
conditions that eliminate the risk of bacterial contamination. They
can be used under physico-chemical conditions corresponding to
multiple processes used by the textile, leather, cosmetic or
pharmaceutical industries. Because of their originality, abundance
and the many interactions and symbioses that govern the dynamics of
bacterial and Archaean communities in extreme environments, these
microbes represent a largely unexplored genetic resource (Figure
7). Thus, the search for new biocatalysts and antibiotics based on
the microbial biodiversity of extreme environments is a rapidly
expanding discipline requiring the development of dedicated
enzymatic and structural screening and characterization
platforms.
Conclusion
Extremozymes obtained from extremophiles have a great economic
potential in many industrial processes, including agricultural,
chemical and pharmaceutical applications. Many consumer products
will increasingly benefit from the addition or exploitation of
extremozymes. It has been suggested that less than 10% of the
organism in a defined environment will be cultivatable and so
further improvement of gene expression technologies (e.g., by the
development of novel and improved heterologous host systems) will
accelerate the exploration of microbial diversity. These
extremozymes will be used in novel biocatalytic processes that are
faster, more accurate specific and environmentally friendly.
Concurrent developments of protein engineering and directed
evolution technologies will result in further tailoring and
improving biocatalytic traits which will increase the application
of enzymes from extremophiles in industry.
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