Winter has long reigned in the globe’s northern latitudes, where vast expanses of frozen soils called permafrost nurture a rich, if still mysterious, mix of microbes that can tolerate year-round subzero temperatures. But as climate change warms the permafrost, that microbe community is changing in ways scientists are still trying to understand. Most worrisome is what will happen to the permafrost’s huge store of long-frozen carbon that newly awakened microbes can now feast on, and how that may propel further changes in climate.
Janet K. Jansson, a microbial ecologist at the Pacific Northwest National Laboratory in Richland, Washington, was one of the first scientists to study how the bacterial community in permafrost has shifted as the soils have thawed. Understanding the complexity of life in soils — permafrost or other — has long been made difficult by the fact that scientists are unable to culture a majority of the species that grow there in the lab. But Jansson and her collaborators have found a way to take a molecular census of these exotic organisms to better track changes in soil communities affected by climate change, including the icy north as well as grasslands in the south.
Metagenomics — a technique in which scientists isolate, sequence and analyze DNA of microbial communities directly from the environment — and other molecular technologies, termed “omics,” are offering new insights about underground life and the transformations wreaked by warming temperatures, Jansson described earlier this year at a meeting of the American Association for the Advancement of Science held in Washington, DC, and in a paper she coauthored in the 2016 Annual Review of Earth and Planetary Sciences.
She recently spoke with Knowable about soil critters and how they are adjusting to a warming planet.
This conversation has been edited for length and clarity.
Why is so much still unknown about the soil’s microbes?
For a very long time, the microbes that have lived in the soil, especially in extreme environments, have been difficult to study because they don’t grow well under laboratory conditions. Now we’re starting to be able to look into this “black box” — the soil microbiome — and start to understand what the microbes are doing, and how they’re influenced by the environment. And that’s exciting because once we have that knowledge, we can start to use soil microorganisms to potentially help mitigate the negative impacts of environmental change.
You’ve spent many years studying one example of an extreme soil environment — the permafrost. What makes the microorganisms there distinct?
Permafrost is a special environment. A large fraction of the terrestrial carbon is trapped in the world’s permafrost — about as much carbon as is currently in the atmosphere and in plants combined. The permafrost is like a huge carbon freezer.
What’s really important is that as the permafrost starts to thaw, the microbes that are there start to become more active and metabolize the carbon compounds stored in the soil. And as they degrade them, the microbes produce greenhouse gases like carbon dioxide and methane, which get released into the atmosphere and can drive further warming.
Permafrost is covered by a layer of soil active with microbial life and is characterized by high amounts of carbon (brown) and liquid water (blue), but low levels of oxygen (green). When permafrost thaws in lowlands, more water and less oxygen are available, creating the perfect conditions for anaerobic bacteria to thrive. As a result, the soil community fixes less nitrogen and releases more carbon dioxide and methane into the atmosphere. At higher elevations, however, permafrost thawing can increase soil porosity, which allows oxygen to penetrate farther down. In this condition, aerobic bacteria thrive and release carbon dioxide to the atmosphere. In both scenarios, greenhouse gas output increases as the frozen soils warm.
Bacteria, in the permafrost or elsewhere, all need carbon to grow and produce cellular biomass. But they have other ways to get energy. One of our more unexpected findings were a lot of proteins for the reduction of iron within the frozen permafrost. Microbes can reduce iron for energy — it’s a process that can occur under conditions with no oxygen, but usually requires liquid water.
We were able to replicate this in the laboratory and show that iron reduction is carried out by organisms living in frozen soil. This was key to understand how they survive and — slowly — grow in such low temperatures with little oxygen. It turns out that at subzero conditions it is still possible to have liquid water because salts become concentrated and lower the freezing point of water. So the proteins we found were probably produced by the active iron-reducing bacteria living in salt brines.
How is the polar microbial community responding to warming temperatures?
We’re doing incubations in the laboratory and monitoring in field areas where the permafrost has already started to thaw. I have collaborations with scientists from several different areas in the Arctic: Svalbard, Greenland and Alaska.
What we and others have found is that, as permafrost thaws, the microorganisms that are there start to change — it’s a real turnover. You get a different composition of microorganisms, more of the ones that are better adapted to degrading carbon versus other types of metabolisms. We see a shift in function toward fermentation processes or methane generation. Methanogens — bacteria that produce methane — often increase in numbers. And that makes sense because they now have access to it, if you compare them to the microorganisms in frozen permafrost.
Using our molecular tools, we see not only which organisms are there, but also what pathways they’re expressing to be able to produce these gases. This is important because methane is a potent greenhouse gas and its production can amplify global warming.
One way to see into the black box that is the soil microbiome is by using “meta-omics” — a range of different biological censuses. How can each “omic” help us understand the microbes’ functions?
Each “omic” technology gives you a slightly different view. You start, on one end, by looking at the DNA in the genomes. For these types of organisms, their identity is all about the total number of genes and the type of genes they have — that’s how we know who’s there. But you don’t know if those genes are all expressed or not. The genomic view just shows you what they are potentially capable of doing.
Scientists use a repertoire of molecular techniques to paint a more complete picture of the make-up and dynamics of the soil microbiome. The concept of the metaphenome of the community arises from combining these separate analyses with information about the local environment and other factors.
If you go to the next step, you can look at which organisms are actively transcribing which genes into RNA, what’s called the transcriptome. This gives us a clue about metabolic processes that are active at a given time, and which ones are favored under different conditions.
The next step is the proteome, because not all expressed genes actually are translated into proteins. So, if you look at the proteins that’s an even better confirmation that the expressed genes are dictating the functions that were carried out in that environment, at that particular point in time.
And then, the last step in this “omic” pipeline would be the metabolome. Metabolites — the intermediate molecules of microbial metabolism — are very valuable, because detecting specific metabolites gives us clues about all the biochemical reactions that are occurring in the environment. They are the ultimate signature of the metabolic processes carried out by the microbial community.
To understand how microbes living in one particular environment change as a whole, you’re looking at something called the metaphenome. Can you describe what that is?
The metaphenome is a new concept. It’s a term that represents the combined biological functions, such as using iron for energy or carbon for growth, carried out by all the microorganisms living in a community. You can think of a single organism that has a genome and depending on the resources available or the environment, certain genes are expressed into RNA, but not all — it depends on the situation and can change over time.
If you look at the whole community, that would be a metaphenome: the product of all of those functions carried out by all the microorganisms. Studying that will allow us to predict the impact of environmental change on the microbiome, as well as think of new ways to manage our soil.
What do we know about the role of viruses and fungi in the soil?
We have a big research push right now on the soil virome — the collection of DNA and RNA from all the viruses in a given spot — and that is very exciting. We screened for hundreds and hundreds of soil metagenomes and we were able to find what types of viruses are there. Some of these viruses contain metabolic genes that could potentially help with nutrient cycling in soil.
The viruses are probably really important, and we just don’t know much about them. It is definitely a new frontier because these viruses outnumber all of the other organisms that you have in soil.
We’re also looking at fungi in grasslands, and one of the things we’re really interested in is that when the soil starts to dry, the water no longer connects different locations in the soil. The microorganisms need water to be able to exchange metabolites and interact with each other. So, in dry soils, you have these disconnected “islands” of microorganisms. But fungi can grow these long filaments, called hyphae, that can bridge these disconnected islands and serve as the train for carrying nutrients back and forth between bacteria and to other organisms in the system.
Droughts change the soil microbiome in subtle and not so subtle ways. In grasslands, for example, groups of soil bacteria normally communicate with one another by sending chemical messages through water and through fungal threads called hyphae. In a drought, however, hyphae may be the only option for communicating across long distances. Metabolic interactions within the soil community release carbon dioxide.
The soils of grasslands are another ecosystem you study. How are the microbes there faring with climate change?
I’m concerned about how climate change will affect these highly productive regions of the world, especially with increasing droughts.
Looking at the metaphenome, and the influence of the soil drying on the metagenome, we have found that the microbial community starts to shift its metabolism toward the production of metabolites that help them survive dryness, like sugars and different kinds of osmolites, molecules that help keep the cells from bursting when the soil gets dry.
The thing that really impresses me is that we can now look at a whole community and dissect what the community is doing in response to drought.
What other big questions are you trying to answer?
One of them is: How do these microorganisms across different kingdoms — the bacteria, viruses and fungi — live together in the same system and interact? We don’t know how, because most studies have looked at a single or a couple of organisms in isolation. So how are they functioning as a community? That’s one of our big questions. And then, of course, the second one is: How are these community interactions impacted by climate change or by access to different kinds of resources, like water?
Have these findings changed your view of the Earth’s soil?
I do not consider soil to be dirt, let’s put it that way. It is one of our most precious resources on the planet. Improper land management, such as over-tillage and leaving the soil barren and free of plants, is a problem because it causes erosion. And that happens at a faster rate than new soil is being formed.
We have to conserve our soils. They are alive — they carry billions and billions of microorganisms in a single gram. So, this is a living resource that we have to protect from being eroded and degraded.
