Microbes in Thawing Permafrost: Harbingers of Doom, Salvation, or Something In-between?
"Drill Team" by Katie Sipes, photograph courtesy of the author
Climate change increases the average temperature on Earth, but its myriad effects on Earth’s ecological systems are more complicated to predict. One of the shifts resulting from climate change is the steady and gradual thaw of permafrost, but the complexity of this process means that it has unclear ramifications for our planet. Permafrost is defined as soil that has been frozen continuously for at least two years. The only places cold enough on Earth to maintain permanently frozen soils are the polar regions, some high-altitude locations, and cold parts of the seafloor. Altogether permafrost accounts for roughly a third of global soil organic carbon stocks within the top 3 meters of soil (Tarnocai et al., 2007; Schuur et al., 2015). And much of this soil is thawing. Quickly. The US Environmental Protection Agency recently released a report showing that over the past 42 years, almost all the soil across Alaska has continually increased in temperature, with the more northern parts experiencing even greater warming (EPA website, 2021). This agrees with observations across other arctic locations in Canada and Russia, meaning that this big thaw is a global phenomenon. Thawing permafrost is a problem for a couple of reasons. It results in slumping and compaction of the soils, causing major problems for buildings built on permafrost and for the people who live in these areas. Another potential problem is that the vast quantities of carbon previously locked up in this permafrost might convert to greenhouse gases when it thaws. Soils everywhere are filled with a wide variety of tiny microbes. Despite being frozen, permafrost is no exception. The microbes in permafrost can perform chemical reactions that are positive feedbacks on climate change. Other types of microbes perform chemical reactions that are negative feedbacks on climate change (Graham et al., 2012). The question is: which of the two will win after the thaw?
Some microbes can “eat” the natural organic matter that is abundant in soil and turn it into greenhouse gases such as carbon dioxide and methane. This creates a positive feedback on climate change because, as the permafrost thaws due to increases in greenhouse gases, the microbes in the permafrost will release more of those gases. But other soil microbes consume the greenhouse gases. Some of them can pull in carbon dioxide from the atmosphere and turn it into new organic matter. These are a potential negative feedback on climate change because they provide a sink for greenhouse gases in thawing permafrost. No matter where you are on the planet, the soil microbes are diverse so predicting what they’re going to do is complicated. For this reason, we cannot say which scenario – the positive or the negative feedback on climate change – will dominate in different types of permafrost. But the first step in figuring out how microbes will react to being thawed is learning about which of them are actually in the permanently frozen parts of permafrost to begin with.
Permafrost is frozen year-round, but the soil sitting on top of it is not. The upper section thaws every summer and then refreezes in the winter and is called the active layer. Every summer water trickles through the active layer and pools down on the permafrost layer, leaving ice at the interface in the winter months. This water carries nutrients and microbes from the active layer onto the surface of the permafrost. So, really, thawing permafrost can be more accurately viewed as an increase in the depth of the active layer. Every summer, deeper soils thaw and then refreeze in the winter. It would be a reasonable first guess that a completely frozen block of soil does not have any living microbes in it, . Bbecause, as far as we know, all living things, including microbes, need liquid water. However, we’re learning that permafrost may, in fact, contain small amounts of liquid waterthe reality is more complicated. When soils freeze, pure water collects into ice crystals, leaving any salts that were dissolved in the water behind (Gilichinsky et al., 2007). As water molecules gradually join the ice crystals, the left-behind water gets increasingly salty. Anyone who has spread salt on a freezing sidewalk knows that this lowers the freezing temperature of water allowing it to remain liquid at lower temperatures. Microbes, it turns out, are very good at dealing with high salt concentrations. So, they can survive in the small pockets of salty water that are embedded throughout permafrost. There’s even good evidence that they can live like this for an extremely long time period. Permafrost that has been frozen for tens of thousands to a million years shows good signs of harboring living intact microbial cells (Liang et al., n.d.; MacKelprang et al., 2017; Burkert et al., 2019).
"Happy Dance" by James Bradley, photograph courtesy of the author
So, what happens when these living microbial communities thaw? Presumably, they will have plenty of food to eat, due to the natural carbon that’s been locked up and frozen out of their reach for many years. They also will have the nutrients that have been trickling down from the active layer every summer. It is possible that they will be very happy microbes indeed. My team has just started a project to investigate how these microbes turn these nutrients into greenhouse gases, or how they take up greenhouse gases instead. We are collecting permafrost by drilling through the active layer of some of the northernmost permafrost in the world. At 79°N, there’s not much north of our site in Ny Ålesund, Svalbard, besides water – frozen or not. This project is funded by the US Department of Energy and is distributed across the University of Tennessee, Princeton University, Oak Ridge National Laboratory, and the Pacific Northwest National Laboratory. We also have international collaborators at the Alfred Wegener Institute in Potsdam, Germany, the Institute of Physicochemical and Biological Problems of Soil Science in Pushchino, Russia, Queen Mary University in London, UK, and the University of Naples “Federico II” in Naples, Italy. In March 2021, we completed a long covid-19 quarantine in order to be able to safely conduct our field season in Svalbard, with the support of the British Antarctic Survey and the Norwegian Polar Institute. Through incubations of intact permafrost cores, as well as careful examination of the DNA, proteins, carbon uptake rates, and enzyme activity rates of the natural microbial populations, we hope to shed light on this lingering quandary. Will re-activated microbes produce more greenhouse gases, accelerating our march towards a new, hotter climate? Or will they create a small dam against the tide of climate change, gobbling up greenhouse gases before they escape into the atmosphere? Hopefully our research will help us learn the answer.
References
Environmental Protection Agency (EPA). Climate Change Indicators: Permafrost. EPA. Retrieved June 5, 2021: https://www.epa.gov/climate-indicators/climate-change-indicators-permafrost.
Burkert A., Douglas T. A., Waldrop M. P. and Mackelprang R. (2019) Changes in the Active , Dead , and Dormant Microbial Chronosequence. Appl. Environ. Microbiol. 85, e02646-18. https://journals.asm.org/doi/full/10.1128/AEM.02646-18.
Gilichinsky, D. A., Wilson, G. S., Friedmann, E. I., McKay, C. P., Sletten, R. S., Rivkina, E. M., Vishnivetskaya, T. A., Erokhina, L. G., Ivanushkina, N. E., Kochkina, G. A., Shcherbakova, V. A., Soina, V. S., Spirina, E. V., Vorobyova, E. A., Fyodorov-Davydov, D. G., Hallet, B., Ozerskaya, S. M., Sorokovikov, V. A., Laurinavichyus, K. S., Shatilovich, A. V., … Tiedje, J. M. (2007). Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology, 7(2), 275–311. https://doi.org/10.1089/ast.2006.0012.
Graham D. E., Wallenstein M. D., Vishnivetskaya T. A., Waldrop M. P., Phelps T. J., Pfiffner S. M., Onstott T. C., Whyte L. G., Rivkina E. M., Gilichinsky D. A., Elias D. A., MacKelprang R., Verberkmoes N. C., Hettich R. L., Wagner D., Wullschleger S. D. and Jansson J. K. (2012) Microbes in thawing permafrost: The unknown variable in the climate change equation. ISME J. 6, 709–712.: http://dx.doi.org/10.1038/ismej.2011.163.
Liang R., Lau M., Vishnivetskaya T. A., Lloyd K. G., Wang W., Wiggins J., Miller J., Pfiffner S., Rivkina E. M. and Onstott T. C. (2019) Predominance of anaerobic, spore-forming bacteria in metabolically active microbial communities from ancient Siberian permafrost. , 1–41. https://journals.asm.org/doi/full/10.1128/AEM.00560-19.
MacKelprang R., Burkert A., Haw M., Mahendrarajah T., Conaway C. H., Douglas T. A. and Waldrop M. P. (2017) Microbial survival strategies in ancient permafrost: Insights from metagenomics. ISME J. 11, 2305–2318. http://dx.doi.org/10.1038/ismej.2017.93.
Schuur E. A. G., McGuire A. D., Schädel C., Grosse G., Harden J. W., Hayes D. J., Hugelius G., Koven C. D., Kuhry P., Lawrence D. M., Natali S. M., Olefeldt D., Romanovsky V. E., Schaefer K., Turetsky M. R., Treat C. C. and Vonk J. E. (2015) Climate change and the permafrost carbon feedback. Nature 520, 171–179. https://www.nature.com/articles/nature14338.
Tarnocai C., Canadell G., Schuur E. A. G., Kuhry P., Mazhitova G. and Zimov S. (2007) Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem. Cycles 23, GB2023. https://agupubs.onlinelibrary.wiley.com/doi/full/10.1029/2008GB003327
Karen G. Lloyd is an Associate Professor in the Microbiology Department at the University of Tennessee. She studies microbes "in the wild" in Arctic permafrost, deep-sea sediments, and deeply-sourced hot springs. You can learn more about her work from her TED talks (https://tinyurl.com/8vnh33jh and https://tinyurl.com/epsy6m8) or from her website (http://lloydlab.utk.edu). You can find resources to support the undoing of years of exclusion of Black people in geoscience through Black in Geoscience (https://blackingeoscience.org/) and the National Association of Black Geoscientists (https://www.americangeosciences.org/society/national-association-black-geoscientists).
(c) 2021 Karen G. Lloyd