Montana State research team publishes paradigm-challenging discovery in a Yellowstone thermophile

BOZEMAN – Montana State University has long been a hub for research on the many unique features of nearby Yellowstone National Park, and now a doctoral student in one the university’s microbiology laboratories has published a paper on how some hot-spring-dwelling organisms thrive in their extreme environments.

Lisa Keller, a graduate student who is expected to complete her doctoral studies this spring, is the lead author of a new paper in the journal Nature Communications along with her adviser and mentor Eric Boyd, professor in the College of Agriculture’s Department of Microbiology and Cell Biology. The paper, titled “Simultaneous aerobic and anaerobic respiration in hot spring chemolithotrophic bacteria,” was published Jan. 27.

Keller was working with bacterial samples from a group called Aquificales, which were isolated from a Yellowstone hot spring. She experimented with various conditions to identify how the organisms could best be grown in the lab for further study. Inspired by previous research that showed Aquificales could grow using elemental sulfur, hydrogen and oxygen, Keller began exploring whether various combinations of these compounds could support growth, specifically at the level of cellular respiration.

Cells respire, or breathe, oxygen or alternatives to oxygen through aerobic and anaerobic respiration, respectively. However, they are not known to do both at the same time. At least, that was the prevailing thought.

“One example that people are familiar with is the cells that comprise our own muscles. Our muscle cells utilize a lot of oxygen when we're doing endurance exercise but if our exercise level is too intense, our bodies cannot deliver oxygen to our cells fast enough. So, our cells switch to anaerobic metabolism that causes a burning sensation due to the buildup of lactic acid,” Keller said. “So, it's well known that cells switch back and forth between aerobic and anaerobic metabolism, but they are not known to conduct both forms at the same time.”

Keller cultivated the bacteria in the lab, observing the levels of sulfur and oxygen in the experiment over time. She knew that Aquificales had the genetics necessary for both anaerobic and aerobic metabolism, but as she measured the amounts of sulfur and oxygen, she found that while sulfide was increasing, oxygen was decreasing. That meant that while the bacteria were producing sulfide – an anaerobic process – they were using oxygen, meaning that both metabolisms were occurring.

“There’s no explanation other than that these cells are breathing oxygen at the same time that they are breathing elemental sulfur,” she said.

Keller said the bacterium’s ability to conduct both processes at once challenges our understanding of how microbes survive, especially in dynamic, low-oxygen environments such as hot springs. Many of the organisms found in Yellowstone’s hot springs are ancient lifeforms that reflect life on early Earth when there was no oxygen. The results of this study shed potential light on how ancient lifeforms adapted to the progressive oxygenation of Earth that began around 2.8 billion years ago.

“This is really interesting, and it creates so many more questions,” Keller said. “We don't know how widespread this is, but it opens the door for a lot of exploring.”

Keller, who received her undergraduate degree in microbiology from North Carolina State University, began her doctoral studies in Boyd’s lab in 2019. As she prepares to defend her thesis in April, she hopes to continue pursuing research in the Yellowstone region beyond her graduation.

Boyd has been studying microbial processes and geobiology at MSU for more than 20 years, during which he has received major research grants from the Keck Foundation, the National Science Foundation, NASA, the U.S. Department of Energy and others. He has mentored 27 graduate students and more than 50 undergraduate students, and his lab’s work has been featured in The New York Times – of which Keller was a part – on PBS and in many of the world’s most respected academic journals. Last year, two other members of Boyd’s lab, doctoral students Erica Antill and Alexis McDonnell, received NASA FINESST grants, one of the association’s most prestigious awards.

Boyd said that Keller has been a particularly driven and inquisitive scientist.

“Lisa is a curious person who, through meticulous experimentation, identified a unique phenomenon and then put the time and effort into what would become a paradigm-challenging discovery,” he said, adding that foundational research such as Keller’s can have far-reaching benefits to science and society. “She now gets to reap the rewards of her hard work with its publication in the prestigious journal Nature Communications. Mark my word that this will be one of many top-tier papers that Lisa contributes to science over her career.”

Looking back on her studies, Keller can see how much she has grown as a scientist, writer and communicator, and credits much of that to Boyd’s commitment to high-level mentorship to both undergraduate and graduate researchers.

“He really cares deeply about his students, and he really wants us to succeed,” she said. “He also dedicates so much time and effort into mentoring us and getting us to ask the right questions, teaching us how to think about experiments, how to communicate our science to a broad audience. I really respect the way that he thinks about science, and I feel like I still have so much to learn.”