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Living the Hot Life

Studies of Yellowstone microbes shed light 
on long-standing evolutionary questions

Yellowstone hot pool photo by Patrick Hutchins, Odd Angle Photography

By Chad Dundas

You can tell Scott Miller is used to the question. When you ask it, he leans back in his chair and flashes the sort of patient, accommodating grin that takes years to master.

“What do you do?” he repeats, like he’s heard this one a million times before. “What exactly do you do?”

Such is life for a microbiologist, a guy who has devoted his career to studying creatures the naked eye can’t see — organisms some people are unaware even exist.

Miller’s research into photosynthetic bacterial life in the hot pools of Yellowstone National Park isn’t the kind of thing that’s necessarily easy to explain at cocktail parties. Yet there is magic in Miller’s work.

UM microbiologist Scott Miller investigates the evolutionary mechanisms used by cyanobacterium to adapt to extreme environments.For nearly 20 years the affable associate professor at UM has, among other things, dedicated himself to rooting out the inner life of Synechococcus, a cyanobacterium (or what the layperson might call a “blue-green alga”), that holds the record for temperature tolerance by a photosynthetic organism. In an attempt to understand how these microorganisms are able to not only survive but also thrive in hot springs at temperatures up to 165 degrees Fahrenheit, Miller and his research team are chipping away at some of evolutionary biology’s enduring and fundamental puzzles.

“We’re specifically looking at adaptation to extreme environments,” he says. “But the thing that really motivates me and drives me is trying to answer some very general but long-standing questions about evolution. What is the stuff of adaptation? Is it new mutations? Is it pre-existing variation that is out there in the environment that gets co-opted and harnessed for adaptation? Does adaptation to higher temperatures come with a cost?”

In his sparse office inside UM’s Health Sciences Building, the desktop of Miller’s computer displays a well-known aerial photo of Yellowstone’s Grand Prismatic Hot Spring. At first glance it looks like something out of a science fiction movie — a lake with an electric blue center that fades to shades of yellow, orange and black as it reaches the edges. Miller runs his finger around the outside rim of the hot pool, explaining that its rainbow assortment of colors primarily are produced by cyanobacteria, and that different varieties — or genetic variants — of Synechococcus can be found within different hues, with the yellow ring representing the “tree line for photosynthesis as a way of making a living.”

Miller’s research seeks to shed light on numerous questions about how and why these specific cyanobacteria have been able to adapt to life in extreme environments, as well as why there are so many different varieties of Synechococcus living at different temperatures. It’s work that could inform not only our understanding of the evolutionary process but also could someday have biotechnological applications.

In January, along with co-authors Michele McGuirl and Darla Carvey, Miller published an article in Molecular Biology and Evolution that began to unlock some of the mystery.

Miller says that before he came to UM a decade ago, more of his work was conducted in the field, traveling to hot springs in Yellowstone and Oregon to collect study samples in order to piece together how different Synechococcus function and to reconstruct their evolutionary history. In order to really do evolutionary biology, he says, and to understand the path evolution has taken, scientists first need to have a fundamental understanding of how their study organisms are related to one another. Much of his work has involved putting that puzzle together one piece at a time.

Synechococcus, a cyanobacterium, holds the record for heat tolerance by a photosynthetic organism.“Early on there was a lot of fieldwork, growth studies in the lab and building of family trees because we didn’t have a good feel of how these otherwise morphologically identical rods were related to one another or how they differed functionally,” he says. “Nowadays, it’s a very integrated research program. It spans everything from fieldwork to biochemistry to now genomics. We’re not just sequencing single genes and building evolutionary trees, we’re getting entire genomes and using that to understand the history and mechanisms of diversification.”

Recently, the work has involved purifying proteins and using what Miller calls “tricks of molecular biology” to alter genes and make ancestral versions of various enzymes. One such enzyme is RuBisCO, which was the focus of Miller’s recent publication.

RuBisCO (or Ribulose-1, 5-bisphosphate carboxylase oxygenase, if you’re scoring at home) is a common enzyme that exists in both plants and cyanobacteria and is involved in the first step of carbon fixation — the process by which photosynthetic organisms turn carbon dioxide gas into sugar (“The process that built the biosphere,” Miller says).

Using a technique called circular dichroism, Miller’s team determined that the RuBisCO enzyme of the most thermotolerant Synechococcus is more stable than those of other varieties, or of ancestral enzymes they were able to synthesize in the lab. In addition, they were able to determine the specific genetic changes that made this RuBisCO better suited to withstand higher temperatures than its peers. The results yielded fresh insights on our understanding of the process of what the paper calls “niche differentiation and ecosystem function.”

Hunter’s Hot Springs near the Oregon-California border, where many of the organisms Miller studies came from“The magic for me comes from investigating the fundamental question,” Miller says. “We’re trying to figure out whether there are any general mechanisms for evolving environmental tolerance using not just Synechococcus but other cyanobacteria that occupy these extreme environments.”

It is precisely the fact that so little is known about microscopic life in hot springs that drew Miller to the field in the first place. While pursuing a graduate degree at the 

University of Oregon, he was leaning toward a career in freshwater ecology until he took the weekend field trip that changed his life.

During his first quarter at UO, Miller’s freshwater ecology class visited Hunter’s Hot Springs near the Oregon-California border. As he was listening to his instructor give his introductory remarks about the area, which was discovered by the Hudson Bay Company in 1832 and is home to the man-made Old Perpetual geyser, Miller knew he had found his niche.

“That was the first time I ever saw a hot spring,” he says. “Something about it just clicked. We got there, and the professor started talking about all the things we know about this place, but then it gradually came out that we didn’t know all that much after all.”

For an aspiring scientist, that was pretty much all Miller needed to hear.

“It was sort of like a last frontier of biological diversity for me, and I think that’s what captured my fascination,” he says. “I said, ‘Wow, we know hardly anything about these things,’ and I just caught the bug. I really got into microbiology and microbial diversity as a result. I think it was this drive to understand what was there and what they were doing.”

Miller’s team studies hot pool life in places such as the Grand Prismatic Hot Spring in Yellowstone National Park, whose rainbow colors are caused by different genetic variants of Synechococcus. (Photo by Jim Peaco, National Park Service)Ten years later, Miller and his partner, plant evolutionary geneticist Lila Fishman, moved from their positions in the Research Triangle of North Carolina to UM, where their labs are right across the hall from each other. Though Miller remains chiefly interested in the pure science of his work, because the proteins he works on are of economic interest and heat stability is a desirable property in many industrial processes, he admits there might be “serendipitous” biotechnological applications that come along with the discoveries.

Ask him about the progress of his research program, and the accommodating grin returns, now with an unmistakable undercurrent of modesty lighting his eyes.

“The students do all the work,” he says. “I sit behind a desk, mostly. They try to keep me out of the lab. I had pretty good hands once, but now I might be more likely to break some glassware or something whenever I’m allowed to run amok in there. It’s a huge team effort. Excellent people make all this possible.”

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