Like Bill Murray in the movie Groundhog Day, bacteria species in a Wisconsin lake are in a kind of endless loop that they can’t seem to shake. Except in this case, it’s more like Groundhog Year.
According to a new study in Nature Microbiology, researchers found that through the course of a year, most individual species of bacteria in Lake Mendota rapidly evolved, apparently in response to dramatically changing seasons. Gene variants would rise and fall over generations, yet hundreds of separate species would return, almost fully, to near copies of what they had been genetically prior to a thousand or so generations of evolutionary pressures. (Individual microbes have lifespans of only a few days – not whole seasons – so the scientists’ work involved comparing bacterial genomes to examine changes in species over time.) This same seasonal change played out year after year, as if evolution was a movie run back to the beginning each time and played over again, seemingly getting nowhere.
“I was surprised that such a large portion of the bacterial community was undergoing this type of change,” said Robin Rohwer, a postdoctoral researcher who led the research, first as a Ph.D. student working with Trina McMahon at the University of Wisconsin-Madison and now with co-author Brett Baker at The University of Texas at Austin. “I was hoping to observe just a couple of cool examples, but there were literally hundreds.”
Lake Mendota changes a lot from season to season — in the winter, it’s covered in ice and in the summer, it’s covered in algae. Within the same bacterial species, strains that are better adapted to one set of environmental conditions outcompete other strains for a season, while other strains get their chance to shine during different seasons.
The team used a one-of-a-kind archive of 471 water samples collected over the course of 20 years from Lake Mendota by McMahon, Rohwer and other UW-Madison researchers as part of National Science Foundation-funded long-term monitoring projects. For each water sample, they assembled a metagenome, all of the genetic sequences from fragments of DNA contained in bacteria and other organisms captured in the sample. This resulted in the longest metagenome time series ever collected from a natural system. The DNA sequencing was made possible by the Joint Genome Institute in Berkeley, CA, in one of the largest projects ever awarded through their Community Science Program.
“Most scientists study these processes in test tubes,” says McMahon, a professor of bacteriology and civil and environmental engineering at UW-Madison. But, thanks to that unique, 20-year dataset, “this is the first time anyone has documented such clear evidence of ecological dynamics and evolution happening at the same time in “wild” microbes.”
What’s more, McMahon says, what the team of researchers learned about the microbes of Lake Mendota can help inform our understanding of lakes across the globe.
“The bacteria with some of the most interesting changes in their genomes are also the most abundant and also the “cosmopolitan” ones, meaning they have been found in every freshwater lake that anyone has sampled, around the world,” she says. “These bacteria play important roles in “mopping up” dead cyanobacteria and recycling nutrients, which can be both good and bad for water quality.”
In addition to the seasonal shifts in bacterial communities, the study also revealed longer-lasting changes.
In 2012, Lake Mendota experienced unusual conditions: the ice cover melted early, the summer was hotter and drier than usual, the flow of water from a river that feeds into the lake dwindled and algae, which are an important source of organic nitrogen for bacteria, were more scarce than usual. As the team discovered, many of the bacteria in the lake that year experienced a major shift in genes related to nitrogen metabolism, possibly due to the scarcity of algae.
“I thought, out of hundreds of bacteria, I might find one or two with a long-term shift,” Rohwer said. “But instead, 1 in 5 had big sequence changes that played out over years. We were only able to dig deep into one species, but some of those other species probably also had major gene changes.”
The hot, dry summer experienced by Lake Mendota in 2012 is exactly the kind of extreme event predicted to increase in climate change models, which may mean more dramatic shifts in the lake’s microbial community. But, McMahon says, forecasting the fates of bacteria is always a challenge.
“The microbes in Lake Mendota are changing all the time, both in terms of how abundant each one is, but also their genetic capacities,” she says. While 2012 conditions resulted in permanent changes in some species’ genome, other “abundant organisms were very resilient and returned to their original state.”
The study points to a giant puzzle that scientists are starting to piece together thanks to mountains of data collected in the two long-term datasets and, equally important, big advances in computing, McMahon says. The researchers used the supercomputing resources at the Texas Advanced Computing Center (TACC) at UT-Austin to reconstruct bacterial genomes from short sequences of DNA in the water samples. The same work that took a couple of months to complete at TACC would have taken 34 years with a laptop computer, Rohwer estimates, involving over 30,000 genomes from about 2,800 different species.
According to Baker at UT-Austin, the study is a “game-changer” in our understanding of how microbial communities change over time. “This is just the beginning of what these data will tell us about microbial ecology and evolution in nature,” he says.
Other co-authors of the new study are: Mark Kirkpatrick at UT Austin; Sarahi Garcia at Carl von Ossietzky Universität Oldenburg (Germany) and Stockholm University; and Matthew Kellom at the DOE Joint Genome Institute.
This is one of two related papers publishing today in the journal; the companion paper focuses on the ecology and evolution of viruses from the same lake samples. The two papers relied on collaborations among researchers housed in three colleges at UW-Madison: the College of Letters and Sciences, the College of Engineering, and the College of Agricultural and Life Sciences.
Support for this research was provided in part by the U.S. National Science Foundation, U.S. National Institutes of Health, the Office of Science of the U.S. Department of Energy, U.S. Department of Agriculture, the Simons Foundation and the E. Michael and Winona Foster-WARF Wisconsin Idea Graduate Fellowship in Microbiology.
Byline: Marc Airhart (UT-Austin) and Adam Hinterthuer (UW-Madison)
CONTACT:
Robin Rowher – robin (dot) rohwer(at) gmail.com
Trina McMahon – trina (dot) mcmahon (at) wisc.edu