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Extremophilic bacteria: our distant ancestors

Thermophilic and hyperthermophilic archaea and bacteria give us an idea of the conditions under which organisms evolved as long as 3.5 billion years ago. It is still unclear whether the first cells originated on the surface of hot volcanic springs or on hydrothermal vents in oceans.

Hot volcano spring near Sasso Pisano, Toscany © EJ

Germans who want to see close up the extreme conditions under which organisms can thrive tend to travel quite a long way. The Yellowstone National Park in the Rocky Mountains or the Icelandic and New Zealand geyser landscape are probably the best known places. However, there is no need to travel to such distant places, Italy is far enough. The Tuscan village Sasso Pisano along with the Solfatara volcanic crater, which is near Naples, have plenty of lagoons, mud springs and sulphurous exhalations, which bubble eerily and give off a rotten-egg smell. The rims of the springs are covered with yellow, rust-red and lurid green crusts. The heat of the soil can be felt through the thick soles of hiking boots and one has to be careful not to burn one’s feet when approaching the springs.

Thermus aquaticus and ecosystems that are billions of years old

Although these crusts are so conspicuous, it was not until the late 1960s that biologists inspected them closely and discovered that they resulted from the activities of living organisms. The crusts had previously been regarded as pure mineral deposits as it was difficult to imagine that they actually harboured life. In summer 1971, a young microbiologist working as a ranger in the Yellowstone National Park enthusiastically showed me the slimy and colourful deposits of microorganisms on the rim of a steaming lagoon in close vicinity to the famous geyser known as Old Faithful. A couple of years previously, the very same microbiologist and his supervisor Thomas D. Brock from Indiana University in Bloomington, had begun to isolate and characterize these microbes. In 1969, they published their first paper on one such “thermophilic” bacterium, which Brock named Thermus acquaticus. Twenty years after this publication, the bacterium became world famous: Taq, as the bacterium Thermus aquaticus is called by molecular biologists, was used to produce the enzyme Taq polymerase, which is a heat resistant DNA polymerase that became the basis of a method known as polymerase chain reaction (PCR), for which Kary Mullis was awarded the Nobel Prize in 1993.

Crusts and solfataras in a lake in the Yellowstone National Park. © EJ

Nowadays, it would not really be possible to ask a ranger for explanations about the colourful crusts. The rangers all have their hands full keeping the huge numbers of tourists behind the safety barriers at the hot springs. Some years later when I returned to the spot where I had met the young microbiologist, a sign had been erected warning visitors not to harm the fragile ecosystem of the volcanic crusts. This has a rather comic side to it, given the fact that scientists are now convinced that these ecosystems have been around for 3.5 billion years or more and that they will certainly out-survive us humans.

Many microbial species that are adapted to life in the hot volcanic springs have since been characterized. The bacteria are frequently surrounded by a thick protective layer of mucus. They can be discerned with the naked eye because they aggregate into filaments, junks and layers. The orange areas of some lagoons suggest the presence of carotene pigments of Thermus aquaticus which thrives best at temperatures of 70°C; Pyrococcus furiosus bacteria, which are genuine hyperthermophilic organisms, are most at home in the very hot centre of the lagoons. Some microbes use the high temperatures to produce water and methane from carbon dioxide and hydrogen. The colour red suggests the presence of microorganisms that are able to oxidize soluble iron ions (Fe2+) into rust (Fe3+), and the yellow sulphur deposits possibly originate from sulphate-reducing bacteria. In contrast, Sulfolobus solfataricus (named after the aforementioned volcano near Naples) bacteria oxidize elementary sulphur into sulphate and sulphuric acid using carbon dioxide as single carbon source. Karin Lauber from Technische Universität Darmstadt did her doctorate on the sulphur metabolism of Acidianus ambivalens, a hyperthermophilic and extremely acidophilic Sulfolobus relative.

An entirely distinct domain of life

Tree of Life with the three domains: Bacteria, Archaea and Eukaryota © C. Woese
The American microbiologist Carl Woese showed that many microorganisms that are adapted to life in such extreme conditions differ fundamentally in their molecular characteristics from the vast majority of known bacteria. Woese is famous for defining the Archaea (formerly called archaebacteria) as a new domain of life; they are classified as a separate domain in the three-domain system comprising Archaea, Bacteria and Eukaryota (organisms with a real nucleus). Animals, plants and fungi belong to the Eukaryota domain. Archaea differ from bacteria in the composition of their ribosomes, their RNA sequences and in the molecular composition of cell membranes (ether bridges instead of ester bonds). Archaea are found in hot volcanic springs, in nearly saturated brine and in extremely acidic or alkaline environments. Woese named these bacteria Archaea (from the Greek “archaios” = very old) as he believed it to be a very old group of organisms that was adapted to the prevailing conditions on Earth billions of years ago.

Recent investigations have confirmed Woese’s findings. In the tree of life constructed by the Structural and Computational Research group at the European Molecular Biology Laboratory (EMBL) on the basis of genome analyses (see also "Genome analysis leads to a new tree of life"), the Archaea represent an own lineage. Moreover, they seem to be more closely related to eukaryotes (and hence to humans) than bacteria. Previous research had already suggested this possibility. The “signal recognition particles“ (SRPs, ribonucleoproteins that are present in all organisms) of the archaea are more closely related to the SRPs of eukaryotes than to those of bacteria, as has been shown by Irmgard Sinning from the EMBL (now professor at the Biochemistry Centre Heidelberg) and others with Sulfolobus solfataricus. The “elongation factor”, a component of the protein biosynthesis apparatus, and other components that are the basic components of all organisms are also found in archaea. However, it must be pointed out that the similarity of eukaryotes with archaea is limited to the actual eukaryotic cells and their nuclear DNA, but does not apply to mitochondria, which have most likely arisen from the endosymbiotic engulfment of true bacterial cells into an eukaryotic cell (which may derive from an archaeal cell).

Extremophilic representatives are not only found among archaea, but also among bacteria. The best example of extremophilic bacteria is Thermus aquaticus. The British evolutionary researcher Thomas Cavalier-Smith places Thermus aquaticus into a group of bacteria that have particularly primordial characteristics. Cavalier-Smith calls this group “Hadobacteria” (derived from “Hades”, the Greek for underworld) in reference to the hellish conditions in which these organisms evolved at a time which is referred to as the Hadean phase that began with the formation of the Earth around 4.55 billion years ago and ended around 3.9 billion years ago.

Black and white smokers

Black smoker at a depth of 2,000 m in the Mid-Atlantic Ridge © German Aerospace Centre, DLR

When Charles Darwin reflected about the development of life on Earth, he imagined a warm tidal pool on the beach under the hot glowing sun in which the decisive stages of evolution took place. We now believe that the beginning of life started in a bubbly inferno, exposed to meteorite hail, extreme temperatures, intensive UV radiation and a thin atmosphere enriched with methane, ammoniac and other gasses that are toxic to humans. 

Since the so-called black smokers were discovered in the Mid-Atlantic Ridge, many researchers have favoured the idea that it was in these geysers where life on Earth began. By dint of being inside the smokers, the organic structures and cells in the smokers were protected against the deadly ionizing radiation on the Earth’s surface. Black smokers are hydrothermal vents with a cylindrical chimney structure that arise from sulphur, iron and other minerals that are dissolved in the super-heated vent water as it comes into contact with ice-cold sea water. In early 2012, hydrothermal vents were discovered in the Caiman Trough at a depth of 5,000 m below sea level. They eject water at temperatures exceeding 450°C and pressures of 500 bar to a height of around 1,000 m. A rich, bizarre and completely autonomous ecosystem has developed around such black smokers, including colourless shells, snails, crustaceans, fish and many other organisms. The most conspicuous species is a spaghetti-like giant tube worm with a dark red front, 3 m long and 4 cm thick (Riftia pachyptila). The worms have no intestines; they feed exclusively on chemosymbiotic microorganisms.

“Strain 121“ holds the record for sustaining life at the highest temperature. The negatively stained electron microscope image shown on the right reveals iron deposits formed by archaea. © K. Kashefi, University of Massachusetts, Amherst

The ecosystems around the hydrothermal vents depend on the presence of extremophilic archaea and bacteria that derive their energy from the dissolved minerals. A couple of years ago, an iron-reducing archaea specimen was discovered at a black smoker in the North-East Pacific, which thrived at a temperature of 121°C, the highest temperature ever found to harbour life. When the temperature was increased to 130°C in the laboratory, the microbe “Strain 121” stopped growing, but could be resuscitated in boiling sea water.

Some scientists have recently come to suspect that microorganisms’ ability to live in extreme temperatures is a secondary adaptation rather than a leftover from the time when the Earth first came into existence. The researchers believe that life develops better in the vicinity of what they call white smokers. White smokers are hydrothermal vents with temperatures that are lower than those of black smokers. They emit water that is rich in minerals such as sulphate and silicon. White smokers, more of which are continuously being discovered, also provide a starting point for a more complex ecosystem based on the presence of chemolithotrophic bacteria and archaea.

The oldest traces of life (sterane molecules with a carbon isotope ratio which, according to modern knowledge, can only be formed by living organisms) were discovered in the oldest known rock, i.e. in the Isua serpentinit (around 3.8 billion years old) on Greenland, which contains carbon-rich alkaline compounds like the ones produced in hydrothermal sea springs at temperatures between 100 and 300°C. Whether they are looking at black or white smokers, undersea geysers or geysers on the Earth’s surface, researchers all agree that the first organisms on Earth very probably had the same characteristics as modern extremophilic archaea and bacteria.

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