Soil Microbes Sacrifice Ribosomes in Response to Warming

Sustained increases in soil temperature cause microbes to dial down protein synthesis over the course of years but potentially on the scale of weeks. At the same time, warming microbial populations increase their carbon dioxide production and growth rate, a study published in Science Advances on March 25 shows, suggesting that bacteria can adapt to changing environments, maintaining a high rate of cell division in the face of warmer conditions.

The study finds that “warming of any duration appears to lead to reduced need to invest in protein machinery, since the kinetic energy of warming accelerates enzymatic and metabolic rates in a compensatory way,” Kristen DeAngelis, a microbiologist at the University of Massachusetts, Amherst, who was not involved in this study, writes in an email to The Scientist. “This is a really exciting observation, and presumably one that should be generalizable across systems, not just to soils.”

In order to measure how microbial activity changes over time, the study authors made use of the longest running experiment exploring soil warming in situ, called ForHot, in which researchers have monitored a grassland in the subarctic region of Iceland that has experienced geothermal soil warming for more than 50 years. Additionally, to investigate how soil microbes respond to warming on shorter timescales, the researchers also studied microbes at a site nearby, where an earthquake in 2008 transported one of the geothermal channels to a new location. This presented the opportunity to study a newly formed heat gradient in addition to the historical site. “It could be a peek into how future global warming is going to affect soils,” Alexander Tveit, a microbiologist at The Arctic University of Norway who led the study, tells The Scientist. 

See “Arctic Swelters Under 38 °C Heat Wave”

To understand how bacterial communities respond to warming from a functional standpoint, the researchers turned to high-throughput shotgun sequencing of total RNA. With this metatranscriptomics approach, they were able to study a wide variety of the organisms found in the soil microbiome simultaneously, comparing which genes were expressed differently when the soil was warmer than usual. The researchers obtained samples from both ends of the decades-old temperature gradient and of the gradient formed after the 2008 earthquake: they took four samples from one end of each gradient, where soil sat at ambient temperature, and four samples from the other end, where soil had been heated to more than 6 °C above ambient temperature through geothermal warming.

It could be a peek into how future global warming is going to affect soils.

—Alexander Tveit, The Arctic University of Norway

Looking at the total RNA extracted from each of the 16 samples, the researchers found that “the amount of RNA in the soil is lower in the warm [soil], Tveit says, indicating reduced protein synthesis. “Even if the microbial biomass is not changing—or changing very little—the RNA content is going down,” Tveit adds. Sequencing showed that the protein biosynthesis machinery, particularly ribosomal proteins, was downregulated in bacterial communities in warm soil. “The main finding of this study is that genes associated with the synthesis of proteins were down-regulated under warmer conditions,” Sylvain Monteux, a microbial ecologist at Stockholm University who was not involved in the study, writes in an email to The Scientist. “Importantly, they could show that this was not due to a change in microbial community structure, so while the same microbes are present it’s their activity that is changing.”

See “Warming Permafrost Morphs Microbes into Greenhouse Gas Emitters”

To the authors, these observations suggest that ribosomal content is reduced in bacteria in warmer soils compared to bacteria in cooler soils. Typically, that would be detrimental to the bacteria’s survival, but this seems to not be the case because the bacterial communities in warming soils had higher biochemical reaction rates at higher temperatures, Tveit says. “When it gets warmer, the organisms and all their enzymes will work faster,” allowing the microbes to sacrifice ribosomes but still maintain high metabolic and cell division rates, even as they deplete soil carbon more rapidly than normal, Tveit argues. “They can sustain a high growth rate and high rate of decomposition in the warm soil because they are removing parts of themselves—kind of losing weight—even when the soil contains less nutrients.” These changes appear over the course of months and years, but preliminary evidence presented in the paper indicates that downregulation already occurs after just one week of warming.   

Drawing conclusions about how this phenomenon affects the rates of carbon dioxide released from warming soils and how that feeds into climate change is “a step too far” at the moment, Tveit says. “It will likely enable the organisms to deplete the soil more of carbon than they would have been able to without ribosome regulations. They can keep going at a higher rate for a longer time than they would otherwise [be able to].”

See “Incorporating Soil Microbes in Climate Change Models”

“While these findings need to be confirmed in other soils to assess whether they can be generalized, they represent a decisive step toward a better mechanistic understanding of microbial responses to warming,” writes Monteux. “The fate of soil organic matter and the greenhouse gas emissions that might result from its decomposition in a warmer world has a global reach. And understanding microbial responses to warming is necessary to accurately include it in biogeochemical models.” 

Coauthor Andrea Söllinger, a microbial ecologist at The Arctic University of Norway, is now investigating whether such warming-induced ribosome regulation also happens at a shorter timescale, within weeks and days.—Preliminary experiments also showed that a similar reduction in ribosomes occurs in other types of soils, such as forest soils, says Tveit. “They react to removing their own resources by adjusting the central protein biosynthesis machinery.” 

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