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Fungi erupt on Erebus

Discovery of fungal communities in ice caves highlights human contamination

Researchers have identified more than 60 species of fungi from an ice cave near the top of Mount Erebus, an active volcano in Antarctica. The find demonstrates the hardiness of organisms to survive in extreme environments — and the potential for human contamination in even the most pristine places.

Laurie Connell at the University of Maine and Huber Staudigel with Scripps Institution of Oceanography at the University of California in San Diego published their findings last month in the journal Biology. Connell’s laboratory analyzed soil samples taken from Warren Cave near the top of the 3,794-meter-tall volcano.

It’s the first report of a fungal community being associated with what scientists call a dark oligotrophic volcanic ecosystem (DOVE) in Antarctica. DOVEs are nutrient-poor places in the Earth’s lithosphere, consisting of the crust and upper mantle, where life is able to subsist despite the absence of light for photosynthesis.

“We don’t know how this deep biosphere works with the surface biosphere that we see all the time,” Staudigel said. “We suspect it’s important, but we know very little about it.”

Staudigel is the principal investigator on a five-year field project in Antarctica to examine extreme environments like Mount Erebus to learn more about life in the early stages of Earth, when there would have been few if any sources of organic matter. Instead, microorganisms would have fed on rock minerals or perhaps the noxious gases of a hyper-volcanic young planet.

The ice caves that dot the flanks of Mount Erebus are an ideal place to study such extremophiles.

Gas and steam vent from the sides of Mount Erebus through fissures called fumaroles, sometimes carving out caves just below the ice-crusted surface. Warren Cave is located about 300 meters from the volcano’s rim near an established field camp called Lower Erebus Hut.

Its easy accessibility for scientists and field parties — some visits perhaps dating back to the Heroic Age of Antarctic Exploration during the early 20th century — has made it one of the most visited and studied of the 120 known caves on the volcano. That has also made it more susceptible to human contamination.

About a third of the 61 fungi species that Connell and her team identified represented Malassezia species, fungi that are associated with skin surfaces of animals and require high lipid content for growth.

“I was surprised at [the high diversity] at first, but when I started looking at what we had, I realized we had a lot of things that were human associated,” said Connell, a co-principal investigator on the National Science Foundation-funded project and lead author on the Biology paper.

Until recently, the decades-long research at Mount Erebus, led by Phil Kyle at New Mexico Institute of Mining and Technology (New Mexico Tech), focused on volcanology, geology and related sciences. But now there is a growing awareness by biologists like Connell that the ice caves offer tremendous potential for studying life in extreme environments.

But human contamination, from food scraps to dandruff, has the potential to upset these natural laboratories, Connell said, “because the communities are so tiny there, adding even a small amount of carbon and other nutrients is probably going to impact it significantly.”

Last year, the United States presented a working paper at a meeting of the Antarctic Treaty nations in Hobart, Australia, that urged developing a code of conduct to help manage human impact to the subterranean system on Erebus and other geothermal environments.

In the interim, the National Science Foundation (NSF), which manages the U.S. Antarctic Program (USAP), instituted a moratorium on visits to all ice caves unless for scientific research. Access to pristine caves was restricted except for purposes of collecting data on microbial communities. In those cases, scientists must use clean-access protocols.

Staudigel said development of the protocols is still ongoing in cooperation with members of Kyle’s team, particularly Aaron Curtis, a graduate student at NMT whose research on Erebus has focused on the interplay between the caves and volcano.

“Having protocols in place for newer caves will really change the way we’re working in the caves, but it shouldn’t really change what science we can do,” Connell added. “It will just change the way we’re doing the science.”

During the 2012-13 field season, researchers collected samples from 10 geothermal ice caves on Mount Erebus to determine the current level of microbial contamination. The analyses will focus on using the fungal communities identified by Connell as the smoking gun for human impacts.

In addition to Warren Cave, two other ice caves near Lower Erebus Hut, Hut and Helo caves, have been indentified as likely to be “highly contaminated” from previous visits. At this year’s Antarctic Treaty meeting, the United States and New Zealand pledged to garner more international input into a permanent code of conduct for the Mount Erebus caves and other geothermal sites used for research.

Staudigel said it was important “to protect these environments as much as we can,” while still ensuring the ice caves are available to researchers, as well as others, such as journalists and documentary filmmakers who can help tell the story about such unique places to a bigger audience.

“If we get kids interested in these amazing environments, we might eventually get microbiologists or whatever,” he said. “The excitement that’s involved with the caves is a fantastic [outreach] tool.”

There are already signs that there is an intriguing story to tell about the biology in the Erebus ice caves. Although several of the fungal species found in Warren Cave are cosmopolitan, some have shown to be capable of colonizing minerals and sterile soils, according to the Biology paper.

For example, a species called Aureobasidium pullulans has been identified previously in Antarctica, including from the dry soils in the McMurdo Dry Valleys, and has even been found on the inner part of the Chernobyl inner containment system. An explosion and fire at the Chernobyl Nuclear Power Plant in Ukraine in 1986 created one of the worst nuclear disasters in history.

“The ability to withstand radiation and to withstand desiccation appear to be very similar pathways in some fungi,” Connell said, noting that A. pullulans has even been used in radiation experiments in outer space.

The Biology paper makes further comparisons between the McMurdo Dry Valleys and volcano ice caves. While both ecosystems are low in nutrients, the soil samples from Warren Cave come from a relatively moist, humid and warm environment thanks to the volcanic vent system.

The soils in the Dry Valleys, on the other hand, experience low temperatures and rapid temperate swings, high UV radiation and desiccation.

“It’s a much more benign environment in the caves,” Connell said.

What else might the soils of the volcano ice caves contain? Analyses are continuing at co-principal investigator Bradley Tebo’s lab at Oregon Health and Science University, which is looking at other microorganisms, particularly bacteria.

Samples from Warren cave and others may throw yet more light on the dark ecosystems.

“The fun part is getting [the samples]. The drudge part is doing all the extractions and everything involved to get the data out of them,” Connell said. “The data is the next fun part.”

NSF-funded research in this story: Laurie Connell, University of Maine, Award No. 0739696; Hubert Staudigel, University of California-San Diego Scripps Institute of Oceanography, Award No. 0739712; and Bradley Tebo, Oregon Health and Science University, Award No. 0739731.

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Curator: Peter Rejcek, Antarctic Support Contract | NSF Official: Winifred Reuning, Division of Polar Programs