Mighty Methane-Producing Microbes

April 2014

By SILKE SCHMIDT

A group of microbial organisms called archaea has been the subject of three recent articles related to climate change. All of them were published by international research groups in high-profile scientific journals; and all of them revolved around methane, a carbon-containing greenhouse gas that has 25 times the global warming effect of carbon dioxide (CO2) and is produced by certain types of archaea called methanogens.

In a nutshell, blooms of methanogens in permafrost areas around the world, which are thawing due to warming temperatures, are releasing substantial amounts of methane into the atmosphere, further increasing the speed of global warming (for a video, click here); methanogens as a group respond faster to these rising temperatures than organisms involved in carbon dioxide production or consumption; and methanogens may have been responsible for the largest known mass extinction in our planet’s geological history.

The archaea Methanosarcina seen under a scanning electron microscope. Credit: Power and Syred/SPL
The archaea Methanosarcina seen under a scanning electron microscope. Credit: Power and Syred/SPL

The first of the three studies, published on March 10, 2014, by Nature Communications, was conducted by researchers at the University of Queensland, Australia, and Uppsala University, Sweden. They studied the Stordalen mire in northern Sweden, a massive swampy bog that used to be permafrost: ground that remains frozen year-round. The mire has been thawing for the past 30 years, and this has been accompanied by increasing emissions of methane. To figure out what causes the methane emissions, the researchers analyzed samples of peat, water, and air from the mire.

They found that one particular type of microbe dominated their samples: DNA from the newly named species Methanoflorens stordalenmirensis accounted for 90% of all identified archaea species. Fragments of its DNA had previously been known, but the new study was the first to sequence its entire genome and determine exactly what it does.

M. stordalenmirensis is rarely found in intact permafrost that remains frozen year-round. Instead, it was classified as an indicator species for melting permafrost, which creates acid peatlands that undergo a cycle of freezing, melting, flooding and drought every year. It thrives so much in this unique environment that it forms blooms, similar to algal blooms in freshwater lakes that are too rich in phosphorous and nitrogen; this is a novel observation for methanogens, and it is bad news for our climate.

As a group of microorganisms distinct from bacteria, archaea are billions of years old. Their ancestors flourished in our planet’s oceans long before another important group of microbes called cyanobacteria started to change Earth’s atmosphere by enriching it with oxygen. While this new oxygen-rich climate supported many other life forms, it was not well tolerated by archaea.

However, archaea did not disappear entirely; instead, they took up residence in oxygen-free hiding places, such as permafrost, hot springs, hot dry desert soil, or deep down in the Earth’s crust. The permafrost-dwelling archaea continued to produce methane, but it either stayed below the ice or was promptly consumed by other microbes.

Our warming climate has begun to coax some of these archaea out of their hiding places. The melting permafrost in the Swedish mire and similar areas around the world provides them with better access to carbon dioxide and hydrogen, which they convert into methane. By releasing this methane into the atmosphere, M. stordalenmirensis contributes significantly to global methane production and more global warming, since methane is a greenhouse gas 25 times more powerful than carbon dioxide.

The report indicates that global warming may increase the amount of methane relative to carbon dioxide emitted globally from aquatic ecosystems, terrestrial wetlands and rice paddies. Credit: Dr. Cristian Gudasz
The report indicates that global warming may increase the amount of methane relative to carbon dioxide emitted globally from aquatic ecosystems, terrestrial wetlands and rice paddies. Credit: Dr. Cristian Gudasz

A different set of methanogens resides in freshwater ecosystems, such as natural wetlands and rice paddies, and has been the subject of a second study published in Nature on March 19, 2014, by an international research team led by the University of Exeter, United Kingdom. Unlike the melting permafrost, this environment in and by itself is not new; just like the rest of the world, however, it is exposed to warming global temperatures.

The researchers found that the speed at which microbial methane emissions rise in response to these warming temperatures was the same, regardless of whether they analyzed single species of methanogens, microbial communities or whole ecosystems. They also found that biological processes that produce and consume methane respond much faster to higher temperatures than those that produce and consume carbon dioxide. This means that models of future climate change may have to be modified to account for the previously underestimated contribution of methane to the global carbon cycle.

For each degree that the Earth's temperature rises, the amount of methane entering the atmosphere from microorganisms dwelling in freshwater wetlands will increase several times. 127 freshwater ecosystems, including lakes, swamps, marshes and rice paddies, were analyzed.
For each degree that the Earth’s temperature rises, the amount of methane entering the atmosphere from microorganisms dwelling in freshwater wetlands will increase several times. 127 freshwater ecosystems, including lakes, swamps, marshes and rice paddies, were analyzed.

The third study related to methane-belching archaea, published on March 31, 2014, by the Proceedings of the National Academy of Sciences, implicated the so-called group of Methanosarcina as the likely culprit for the largest of this planet’s five known mass extinctions. A group of Massachusetts Institute of Technology (MIT) and Chinese researchers now blame a sudden and explosive bloom of these methanogens in the world’s oceans for wiping out over 90 percent of all marine species and some 70 percent of land animals about 252 million years ago. By releasing massive amounts of methane into the atmosphere during this “end-Permian” mass extinction, Methanosarcina is believed to have changed both the climate and the ocean chemistry on a global scale.

The research team combined evidence from three different sources to propose this novel hypothesis for explaining the mass extinction. First, they reconstructed the evolutionary history of Methanosarcina by comparing the genomes of 50 related microbes. This analysis indicated that a particular gene was transferred to Methanosarcina from a different bacterium right around 252 million years ago.

This gene transfer was significant because it enabled Methanosarcina to exploit what co-author Gregory Fournier called “a pile of food sitting there,” just waiting to be consumed by some living organism. These previously untapped food sources consisted of carbon-rich organic matter that had accumulated in the ocean sediments over many years prior to the mass extinction and included large quantities of a compound called acetate. The gene transfer gave Methanosarcina the novel ability to process this acetate, thus providing an abundant source of dissolved organic carbon that they could now convert into methane and carbon dioxide.

A second important event was a sudden influx of a nutrient that is usually the limiting factor for Methanosarcina’s growth: nickel. The researchers found evidence for a sharp increase of nickel deposits from a geochemical analysis of ancient Chinese ocean sediments. This observation is best explained by massive volcanic eruptions in Siberia at that same time, about 252 million years ago. Previous hypotheses for the end-Permian mass extinction had implicated these volcanic eruptions as the main culprit, but the new findings demoted their role to more of a partner in crime.

The researchers justified the lesser, though still significant, contribution of the Siberian volcanoes with a third piece of evidence obtained from a more detailed mathematical analysis of carbon isotopes found in the same Chinese ocean sediments: it indicated an exponential, or even faster, increase of carbon-containing gases, such as carbon dioxide and methane, in the ancient atmosphere that also started some 252 million years ago.

According to the researchers, the volcanic eruptions alone would have led to a rapid initial injection of carbon dioxide followed by a gradual decrease; however, their opposite observation of a rapid continuing increase of carbon dioxide can only be explained by an exponential expansion of microbial populations. And the rapid growth, or “bloom,” of methane-generating microbes would have caused a simultaneous increase of methane, along with carbon dioxide.

The three pieces of evidence – gene transfer, sudden nickel influx, and the “signature” of microbial bloom in the ocean sediments – together suggest that the mass extinction may have been caused by an explosive release of carbon dioxide and methane that led to lethally high global warming and long-lasting ocean acidification. Exactly how these dramatic changes led to the demise of many species is still not entirely clear.

Some possible explanations for this “microbial archaeageddon” include suffocation from oxygen depletion, since the extreme global warming may have killed oxygen-producing plants that needed a colder climate; it also would have reduced the solubility of oxygen in seawater. Oxygen depletion would have affected both land and marine animals directly, and might also have increased the production of a poisonous gas called hydrogen sulfide. Marine animals with heavily calcified shells were particularly affected by the mass extinction, which could be explained by ocean acidification causing a loss of their ability to grow these shells.

In summary, the research suggests that archaea as a group may have had a similarly big impact on planet Earth as the cyanobacteria that enriched our atmosphere with oxygen and made possible life as we now know it. Daniel Rothman, the first author of the article, readily admits that the new evidence cannot prove conclusively what caused the dramatic mass extinction 252 million years ago. However, he says, “the cumulative impact of [the three independent pieces of evidence] is much more powerful than any one individually;” together, they “make a strong and consistent case” for a single microbial species playing a much greater role in the mass extinction than previously appreciated.

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