Attention permafrost microbes: iron has entered the group chat

February 9, 2024

Haley Dunleavy

man cutting soil core
Photo by Karl Romanowicz
Karl Romanowicz segments a soil core from the wet sedge tundra at Imnavait Creek, Alaska near Toolik Field Station in July 2019.

When Karl Romanowicz first saw the results from his study on permafrost microbes, he almost didn’t believe them. Romanowicz was conducting an incubation for his doctoral research to track how microbes in different tundra soil layers near Toolik Field Station transition as the permafrost thaws. He hoped this would shed some light on future carbon dynamics of the Arctic. The changes he saw were huge.

“I thought maybe it was contamination,” said Romanowicz, who is now a postdoctoral scholar at the University of Oregon. “But then as I dug into the data, it was like ‘this is a very legitimate response.’”

In 30 days, the incubated permafrost soils underwent a complete and consistent transformation. Two iron-cycling Gammaproteobacteria had taken over. The two bacteria shifted from making up less than 0.1% of the relative diversity of microbial species in the permafrost to then totaling over 65% in the post-thaw community. 

The transition zone, which is the soil between the seasonally thawed active layer and stable permafrost, also saw a similarly large increase in iron-cycling microbes, but not the active layer.

It wasn’t just the microbial communities that had changed, Romanowicz and his collaborators, advisor George Kling and fellow Toolik researcher Byron Crump, found. Microbial function also shifted, showing a similar increase in the abundance of genes associated with iron cycling.

That connection with iron is important for the tundra’s vast stocks of soil carbon, Romanowicz said.

 As permafrost thaws, the once-dormant microbes in previously frozen soils wake up and start to grow. It’s a microbial race to consume the freshly thawed substrate, rich with globally important amounts of carbon. Yet thawing permafrost doesn’t just unlock carbon for decomposers. Soils also become waterlogged, driving anoxic conditions.

While scientists are typically concerned that the resulting conditions will drive anaerobic metabolism and trigger methane emissions, Romanowicz said iron changes things. Thermodynamically, methane metabolism is the “last resort for energy,” he said. “But when you have iron to reduce, it makes more energy for them,” he added. “So it's the more preferential pathway.”

meter long organic soil core laying flat on tundra
Photo by Karl Romanowicz
A field team samples a meter-long organic soil core from Imnavait Creek.

The study, recently published in ISME Communications, reported that the abundance of iron-associated functional genes overshadowed those of the methane-producers, or methanogens.

“There’s actually a decrease in methane-related gene abundance throughout the community, even under conditions where you would expect methane to be produced,” Romanowicz said.

Instead, Romanowicz said an “almost cooperative” cycle formed, where the iron reducer, Rhodoferax sp., converted iron into a product that the oxidizer, Gallionella sp., could use in its metabolism, and vice versa.

These processes likely drove the production of carbon dioxide, rather than the more potent greenhouse gas methane, Romanowicz said, at least for this initial change. When dealing with the large amounts of carbon stored in frozen tundra soils, which greenhouse gas it emerges as from thawing soils matters. Methane has a warming potential of 23 times that of carbon dioxide.

“Eventually, [microbial decomposition] could come back to being methane-dominated through time as things level out,” he said. “But it's definitely going to be some sort of iron-mediated flux in these saturated soils initially [upon thaw].”

man in bug shirt holding corer over his head
Photo by Karl Romanowicz
Research assistant Jason Dobkowski celebrates retrieving the soil auger from the permafrost at Imnavait Creek after it had gotten stuck.

 Romanowicz sampled soils from the Imnavait Creek wet sedge tundra site, located about 10 kilometers east of Toolik Field Station, with the help of a field crew. He said their first attempt in June 2019, when soils were still mostly frozen, was a failure.

“The auger motor died with the soil corer a meter down, and it immediately froze into the soil,” Romanowicz said. “We had to leave it there for a month.” 

Once Romanowicz successfully collected the meter-long organic soil cores from the site in July, he accurately segmented them into three distinct layers — the active layer, the transition zone, and permafrost — thanks to decades-long thaw depth records kept by the Arctic Long Term Ecological Research site. This allowed the team to truly test the effects of thaw on each of these distinct layers, Romanowicz said.

He incubated segments in nearly anoxic conditions at a temperature just warm enough to thaw the soils and compared changes in microbial community and genetic function across soil layers for seven and 30 days. The study reported that neither community nor function changed until the 30-day endpoint. Seven days of thaw wasn’t enough to cause any change in any of the layers, he said.

Romanowicz said that while his findings offer insights into the initial changes that permafrost microbiomes undergo, there’s still much to decipher in the microbial fate of thawing permafrost.

“I want to get to the point where we can predict how the permafrost microbiome will transition into the active layer microbiome,” he said.

Understanding this will be critical for accurately modeling microbial carbon release as permafrost thaws, he said.

He said: “Just because you can tell who's there when it's frozen doesn't mean that they're going to be the ones that are active in the future.”