Geochemist Alexandra Phillips has a soft spot for sulfur. This yellow element is an important macronutrient, and she is trying to understand how it is recycled in the environment. Specifically, she's curious about the sulfur cycle in Earth's ancient oceans about 3 billion years ago.
A study of the Lake Superior sulfur cycle that mimicked ancient Earth's oceans has revealed a new sulfur cycle that emphasizes the role of organic sulfur. The discovery deepens our understanding of early Earth's chemistry and the evolution of microbial life.
Fortunately, the nutrient-poor waters of Lake Superior offer us a glimpse into the past. Phillips, a former postdoctoral researcher at the University of California, Santa Barbara and the University of Minnesota Duluth, said this is a good window. She and her co-authors discovered a new type of sulfur cycle in the lake. Their findings, published in the journal Limnology and Oceanography, focus on the role of organosulfur compounds in this biogeochemical cycle.
Learn about sulfates and hydrogen sulfide
Sulfate ions (SO4) are the most common form of sulfur in the environment and are a major component of seawater. At the bottom of oceans and lakes where oxygen is scarce, some microorganisms make a living by converting sulfate into hydrogen sulfide (H2S). The fate of hydrogen sulfide is complex: It can be rapidly consumed by microorganisms during respiration, or it can remain in sediments for millions of years. Converting sulfate into hydrogen sulfide is a time-honored occupation; genomic evidence suggests that microorganisms began doing this at least 3 billion years ago.
But scientists believe sulfates did not become abundant until about 2.7 billion to 2.4 billion years ago, when photosynthesis by newly evolved cyanobacteria began delivering large amounts of oxygen to the oceans and atmosphere. So where did these ancient microbes get their sulfates?
Alexandra Phillips is a marine and climate scientist with expertise in oceanography, geochemistry and geobiology. Her research focuses on organosulfur in oceans and lakes and how social media can create diverse role models for women in STEM fields. Phillips is also a science communicator and policy official.
The meaning of organic sulfur
To solve this problem, Phillips turned to organosulfur, molecules in which sulfur is bound to carbon compounds. These molecules include sulfatides and sulfur-containing amino acids. In modern oceans, sulfates are almost a million times more abundant than organic sulfur. "But in a system that doesn't have a lot of sulfates, all of a sudden organic sulfur becomes a lot more important," she said.
"For a long time, our thinking has been dominated by what we learned from modern oceans, which are rich in sulfates," said senior author Sergei Katsev, a professor at the University of Minnesota's Great Lakes Observatory. Katsev is a senior scientist on the National Science Foundation-funded project. However, understanding the early Earth requires studying the processes that occurred when sulfates were scarce, and this is where organosulfur can change the entire paradigm.
Models of ancient oceans
Lake Superior has very low sulfate levels, almost one thousandth that of modern oceans. "In terms of sulfates, Lake Superior looks much closer to the oceans of billions of years ago, potentially helping us understand processes that we can't go back in time to observe directly," Phillips said. "Early oceans had very low sulfate content because there was much less free oxygen available to form sulfur dioxide."
The Great Lakes are analogues of ancient oceans, allowing Phillips to see how the sulfur cycle would have worked under similar chemical conditions at the time. Three questions came to her mind:
If sulfate reduction is occurring, which microorganisms are responsible?
If organosulfur fuels this process, what types of compounds do the microorganisms prefer?
What happens to the hydrogen sulfide produced?
Phillips and her collaborators traveled to Lake Superior to trace the journey of organic sulfur from source to sink. The team brought water and sediment samples from two sites back to the lab for analysis: One site had plenty of oxygen in the sediment, the other did not. Sulfate reduction usually occurs where the environment is anoxic. Oxygen is a good resource, so organisms prefer to use oxygen rather than sulfate when possible. The team used shotgun metagenomics to find microbes with genes involved in sulfate reduction. They found abundant microorganisms in layers of sediment where sulfate levels peaked. In total, they found eight sulfate-reducing taxa.
Investigating Organosulfur Preferences
The researchers then set out to determine which organosulfur species the microbes preferred. They provided different microbial communities with different forms of organic sulfur and observed the results. The authors found that most of the sulfate produced by the microbes came from sulfur lipids rather than sulfur amino acids. While this process requires some energy, it's much less than what the microbes would gain from subsequently reducing sulfate to hydrogen sulfide.
Sulfur lipids are not only preferred for this process, but are also more abundant in sediments. Sulfur lipids are produced by other microbial communities and float to the bottom of the lake when they die.
After answering the "who" and "how" questions, Phillips turned his attention to where the hydrogen sulfide went. In modern oceans, hydrogen sulfide can react with iron to form pyrite. But it can also react with organic molecules to form organosulfur compounds. "We were surprised to find that there was a lot of sulfurization of organic matter in the lake," she said. "Organic sulfur is not only a booster for the sulfur cycle, but it is also the ultimate sink for hydrogen sulfide."
Novel sulfur cycle
This cycle - from organic sulfur to sulfate to hydrogen sulfide - was new to the researchers. "Scientists studying aquatic systems need to start considering organic sulfur as a central player," Phillips said. "These compounds could drive the sulfur cycle in nutrient-poor environments like Lake Superior and even in ancient oceans."
"This process may also be important in systems with higher sulfate content. Organic sulfur cycles, like the one we see in Lake Superior, may be ubiquitous in marine and freshwater sediments. But in the ocean, sulfate is so abundant that its behavior masks much of our signal," said senior author Morgan Raven, a biogeochemist at the University of California, Santa Barbara. "Working in low-sulfate Lake Superior allowed us to see the true dynamics of the sedimentary organic sulfur cycle. Organic sulfur appears to serve as an energy source for microbial communities and preserve organic carbon and molecular fossils. Combined, these factors can help scientists understand the evolution of early sulfur-cycling microorganisms and their impact on geochemistry."
Phillips adds that some of the earliest biochemical reactions likely involved sulfur. "We are convinced that sulfur played an important role in truly early metabolism. A better understanding of the sulfur cycle can provide insight into how early life forms exploited this redox chemistry."