Survival at the upper temperature limit - thanks to fast metabolism

Researchers discover new surprising survival strategy of microorganisms at the absolute limit of life.

Summary

A large part of microbial life on our planet takes place in the marine sediments beneath the Earth's surface. With increasing depth, temperatures there rise to ranges of over 80°C, which are considered very hostile to life. Recently, researchers found a small microbial community in sediment cores of the Nankai Trough off the east coast of Japan. It remained unclear how it could survive at the extremely hot temperatures of 120°C prevailing there. This has now been discovered by a large international team, led by Tina Treude, University of California Los Angeles (UCLA), with the participation of Florian Schubert and Jens Kallmeyer from the German Research Centre for Geosciences Potsdam (GFZ), using extremely sensitive radio tracer methods and modelling. According to their findings, the microorganisms can only survive at 120°C because they have an extremely fast metabolism. This ensures that increased heat damage to the cells can be repaired. Their observation contradicts the common opinion that life in the deep biosphere runs at extremely low metabolic rates. The study is published today in the journal Nature Communications and was selected as an Editor's Highlight.

Life at the temperature limit

Microorganisms can survive even more than two kilometres below the seafloor, in sediments more than 100 million years old. However, life becomes increasingly difficult with increasing depth, as there is less organic material suitable for nutrition and energy production, and the sharply rising temperatures increasingly damage the cells of living organisms. Even outside hot but still extremely nutrient-rich black smokers, however, microbes have been detected in the recent past that still survive in 120°C environments. For example, in the sediments of the Nankai Trough.

The Nankai Trough off Cape Muroto on Japan's east coast is a unique place for research on the temperature limits for life: Because temperatures rise with depth below the seabed much faster than usual, boreholes as shallow as 1,177 metres can reach temperatures as high as 120°C. With a water depth of over 4,700 metres, even that is still a technological challenge.

International team with drill vessel and hypersensitive measurement methods

The trip in 2016 with the Japanese drill ship Chikyu was part of a Project of the International Ocean Discovery Program and involved research groups from Japan, Germany, Denmark, Switzerland and the USA. Senior author Tina Treude from UCLA was on board the ship and collected the samples, the main analyses were done by first author Felix Beulig (Uni Bayreuth) and Florian Schubert (GFZ). By measuring the turnover rates using radiotracer methods, they detected various metabolic processes of the microbes: so-called methanogenesis, i.e. the production of methane (Beulig), and sulphate reduction, i.e. the conversion of sulphate into sulphide (Schubert).

For this, sample material is taken from the inside of the sediment core under aseptic conditions and mixed with sterile artificial seawater. This mixture is then amended with radioactive markers which are then metabolized by the microorganisms. In this way, the metabolic products methane and sulphide could be detected.

Despite the high temperatures, the researchers were able to detect microbial cells throughout the sediment core. However, at greater depths, at temperatures above 50°C, their concentration was very low. At 120°C only 10 to 500 cells per cubic centimetre can be found, compared to hundreds of millions or even billions of cells living in one cubic centimetre at the sediment surface. "Detecting the microbes and their metabolism under these conditions is therefore a great challenge; it can only be done with extremely sensitive methods and under extremely clean conditions. In addition, many control measurements have to be made that exclude other effects," explains Florian Schubert, PhD student from the GFZ Geomicrobiology Section. In total, more than 700 samples were measured, including about 200 control measurements. Thermodynamic modelling complemented the lab experiments.

Surprisingly fast metabolism for repairing heat damage

The researchers found that the microorganisms can only survive at the absolute temperature limit for life because they have an extremely fast metabolism. "Our discovery strongly contradicts the common belief that life in the deep underground, the so-called deep biosphere, runs at extremely low metabolic rates. But that only seems to be true until temperatures reach a certain level. Eventually thermal decomposition of biomolecules in the cells becomes so massive that the organisms need an increasingly faster metabolism to repair this damage," Florian Schubert explains. Due to the overall hostile conditions in the deep subsurface only a small population of a few tens to hundreds of cells per cubic centimetre can therefore survive in this biotic fringe.

"We usually only see such high metabolic rates in pure cultures in the laboratory," says Jens Kallmeyer, head of the Aquatic Geochemistry Laboratory and the Radioisotope Laboratory of the Geomicrobiology Section. "Our results manifest what we already described last year: The habitability of the marine subsurface goes far beyond the 80 °C threshold proposed so far."

Original publication: Beulig, F., Schubert, F., Adhikari, R.R. et al. Rapid metabolism fosters microbial survival in the deep, hot subseafloor biosphere. Nat Commun 13, 312 (2022). DOI: 10.1038/s41467-021-27802-7

 

Scientific contact:

M.Sc. Florian Schubert
Section 3.7 Geomicrobiology
Helmholtz Centre Potsdam
GFZ German Research Centre for Geosciences
Telegrafenberg
14473 Potsdam
Phone: +49 331 288-28891
Email: florian.schubert@gfz-potsdam.de

Dr. Jens Kallmeyer
Section 3.7 Geomicrobiology
Helmholtz Centre Potsdam
GFZ German Research Centre for Geosciences
Telegrafenberg
14473 Potsdam
Phone: +49 331 288-28785
Email: jens.kallmeyer@gfz-potsdam.de

Media contact:

Dr. Uta Deffke
Public and Media Relations
Helmholtz Centre Potsdam
GFZ German Research Centre for Geosciences
Telegrafenberg
14473 Potsdam
Phone: +49 331 288-1049
Email: uta.deffke@gfz-potsdam.de

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