Author: Becca Dzombak
Edited by: Zuleirys Santana-Rodriguez, Emily Glass, and Whit Froehlich
In Lake Huron, off the coast of Michigan, lies a window to an ancient world. An underwater sinkhole holds water that’s chemically more similar to the ocean than to the rest of the Great Lakes. Microorganisms (microbes) thought to be very similar to those that thrived on Earth billions of years ago live at the bottom, moving around to chase the light and their preferred water chemistry. Geobiologists and biogeochemists are fascinated by this spot, called Middle Island Sinkhole, and the opportunity it presents to understand how ancient lakes may have supported oxygen-generating microbial communities, contributing to the rise of oxygen in our atmosphere. Using environments like Middle Island Sinkhole can help us understand the conditions in which life evolved on Earth (maybe even giving us hints for what to look for in our search for extraterrestrial life) and predict how carbon cycling in lakes might respond under climate change.
There’s plenty of oxygen around today; our atmosphere is oxidizing, which means oxygen can exchange electrons to make the charge on elements like iron more positive. It’s why a bike sitting outside for months gets rusty. But this wasn’t always the case. Over 2.5 billion years (Ga) ago, there was hardly any oxygen in our atmosphere or oceans (anoxic). It was reducing, the opposite of oxidizing (making elements’ charges more negative). Today, we get reducing conditions in places like swamps and deep in the oceans, where there’s not much oxygen. Around 2.4 Ga, though, something changed. Bacteria that could use sunlight to produce energy – and oxygen – evolved and began pumping oxygen into the atmosphere. These bacteria, called cyanobacteria, and their ability to do photosynthesis were critical to changing the composition of our atmosphere and oceans. Without them, life as we know it may not have evolved at all.
We know these dramatic changes occurred due to evidence in the rock record (such as UV-sensitive atmospheric sulfur, oxygen-sensitive metals like iron preserved in oceans and lakes, and deposits of certain iron minerals), but scientists are still researching how and why oxygen began to accumulate. Unfortunately, we can’t time-travel back to 2.4 Ga to see what the Earth looked like, but we have something that comes close. The cyanobacteria that were so crucial to changing the atmosphere billions of years ago still exist today, with some living in unique spots in our lakes and oceans that scientists think resemble conditions on early Earth. Because these spots are similar to ancient environments, scientists can study the bacteria that live in them, the composition of the waters, and the chemistry of the sediments as a real-time, early Earth experiment.
These systems are called analogue environments. An analogue system is an ecosystem that is thought to be similar enough to some other, separate environment that we can use to answer questions about how that initial system might have worked. Think of it as providing a cross between lab experiments and fieldwork; it has all the complexities of a natural environment (which are often lost in a lab), yet it is well-characterized, allowing us to study or modify specific features. One familiar way analogues are used is in climate studies. We can use previous periods of rapid climate change, constrained by chemical data and climate models, to predict what will happen on modern Earth as carbon dioxide accumulates in the atmosphere. We can also work the other way, using modern environments to think about how similar, ancient environments might have looked and behaved. These systems are powerful tools because while much can be learned from the rock record, some aspects of ecosystems are harder to reconstruct – like water chemistry, the composition of the atmosphere, and cycled nutrients. While each of these are individually important, understanding the whole picture is necessary to understand how biology, chemistry, and geology all interact. Using ecosystems that are active today is crucial because it allows us to examine all of these parts working together in one complex environment. Together, they create a unique fingerprint of who’s there and what’s happening. The better we can define these modern ‘fingerprints,’ the better we can interpret similar ‘fingerprints’ from the past.
There are relatively few places in the world today that we can use as analogues for this period in time. They’re rare because they require unique spatial, biological, and chemical characteristics: they have to be deep enough to limit how much oxygen can dissolve in the water, have enough iron and sulfur present, and host microbial communities that are similar to ancient biospheres. Precambrian analogue lakes have been found in Lake Matano, Indonesia; Lake Cadagno, Switzerland; Brownie Lake, Minnesota; and the Dead and Black Seas. These chemically-stratified lakes provide the opportunity for natural experiments in both chemistry and biology.
Middle Island Sinkhole in Lake Huron, off the eastern coast of Michigan, is another Precambrian analogue. The local bedrock limestone dissolved through time and eventually collapsed, creating a sinkhole like the ones seen on the news in Florida, except this one is underwater. Groundwater flows into the sinkhole, delivering calcium, iron, and sulfur; this gives the sinkhole different water chemistry from the rest of the lake. It’s so different that when the National Oceanic and Atmospheric Administration (NOAA) divers swim down to sample the sediment, they can actually see the difference in water density and feel the groundwater current. Because the sinkhole is deep and separated from the rest of the lake, the water loses oxygen a few meters above the lake bed. These chemical differences allow unique microbial communities (called ‘mats’ because of their tendency to grow in large patches) to thrive and a range of chemical processes to take place beyond oxygenic photosynthesis. In addition to oxygen-producing cyanobacteria, the sinkhole also has sulfur-reducing bacteria, which are an early-evolving type of bacteria that are important for sulfur cycling and thrive in low-oxygen, high-sulfide environments. Sulfide-oxidizing bacteria similar to those found in hydrothermal vents (spots on the ocean floor where hot water and minerals are spewed from the crust) also thrive in the sinkhole. Analyzing how these early microbes cycle elements is crucial for understanding biogeochemical cycling in the sinkhole – which, as an analogue environment, then gives geologists insight into how similar ancient systems could have worked, too. Middle Island Sinkhole is unique in its position within a larger freshwater body, allowing scientists to compare microbes and nutrient cycles in low- and high-oxygen settings.
The scientists* working on the sinkhole are interested in who’s there and what they’re doing, and by ‘they,’ researchers mean microbes. Because the microbial community in the Middle Island Sinkhole is populated by ancient types of bacteria, scientists like Drs. Sharon Grim (Univ. Michigan) and Katy Rico (McGill) are curious about what energy-generating pathways (metabolisms) the community are using. That is – are they doing photosynthesis? Are they using other things, like iron or sulfur, for their energy? How is carbon being cycled through this system? And how is it all recorded in the lake sediment, which is what we’d see in the rock record? Answering these questions is important for knowing how to interpret the chemical records left in rocks, and ultimately for understanding the conditions in which early life evolved on Earth. Middle Island Sinkhole offers scientists a unique testing ground for theories of carbon cycling, metal burial, and microbial interactions.
To answer these questions, Grim, Rico, and a collaborative team of scientists from NOAA and other universities go to the sinkhole every few months to collect new samples. The trained NOAA divers discuss a sampling plan with the scientists prior to going down. Once they’re in the sinkhole, the divers take core samples of the lake bed about a foot long, collecting the purple microbial mat and the dark, organic-rich sediment beneath it. Once they surface, the scientists on the boat make a mad dash to sample the microbial community, seal the cores with duct tape, and freeze them in dry ice before atmospheric oxygen gets into the water. This is to ensure that the redox state of the sample does not change and consequently the microbes don’t adapt from their natural state. Water chemistry – oxygen, acidity, light, etc. – is also measured to track any seasonal changes in the sinkhole.
Once they’re back in the lab, the cores need to be divided. The topmost bit, which holds the microbial mat and is so rich in bacteria that it looks purple, goes to Dr. Grim for analysis. She carefully extracts the microbes’ DNA and uses a suite of computationally-intensive programs to determine not only what types of microbes are present (who’s there?), but also what genes they’re expressing and what proteins they’re producing (what are they doing?). By going further than just seeing what microbes are there, this information adds critical nuance to understanding how this ecosystem functions.
The rest of the core goes to Dr. Rico, who uses a tile cutter to slice the frozen sediment into hockey-puck-sized subsamples. Once those are freeze-dried, she can begin geochemical analyses, measuring carbon, nitrogen, sulfur, and a suite of redox-sensitive elements like iron and molybdenum. Looking at all these elements together allows Dr. Rico to examine redox interactions in the sediment and how carbon burial happens in the sinkhole – that is, is the carbon being buried in microbial matter, or organic matter from the freshwater lake above? It has been assumed that the carbon buried (and preserved) in lake beds would have reflected the microbial community, but Rico is questioning that concept. Together, Grim, Rico, their labmates, and their collaborators are improving our overall ability to interpret the chemical signatures left in lake and marine sediments.
What they’ve found so far is fascinating. The microbial community comprising cyanobacteria, sulfate-reducing bacteria, sulfide-oxidizing bacteria, and others isn’t just diverse in the number of species present – it is remarkably diverse in the metabolisms they utilize, even varying during the day. For example, the cyanobacteria can move to the top of the microbial mat during the day, when the light they need to produce energy is available. However, they are also capable of using either sulfide or water in photosynthesis. In anoxygenic photosynthesis, cyanobacteria do not produce oxygen and instead rely upon sulfide and other reduced sulfur species. When they switch to oxygenic photosynthesis, they make significant amounts of oxygen that other microbes, such as sulfide-oxidizing bacteria, rely upon for their own metabolism. During the night, the cyanobacteria aren’t photosynthesizing, and the sulfide-oxidizing bacteria use what little oxygen is already in the water column produced by the cyanobacteria during the day. And quietly in the background, sulfate-reducing bacteria produce sulfide in the mat and sediment, which is then used by the other microbes to drive their metabolisms. By tag-teaming primary productivity, the microbial mat is busy all day and all night. This interactive relationship between seemingly dissimilar microbes highlights that biology is complex and unpredictable – which, of course, is problematic for geologists who seek to understand biological changes through time. This is where Dr. Grim and other geobiologists step in, disentangling the activities of different microbes and providing critical biological context for the geochemical work. Like the microbes in the sinkhole, it’s a tag-team effort.
In the sediment under the microbial mat, one of Dr. Rico’s main findings is related to oxygen-sensitive trace metals. In the literature, it is often assumed that lakebed sediments reflect the entire water column (i.e., if the sediments look anoxic, then the water column would have been anoxic). However, some of Dr. Rico’s recent work has shown that what is recorded in the sediments may be reflecting only localized signals – that is, rather than recording the whole water column, it is recording the smaller-scale low-oxygen conditions in the sediments. Conversely, the carbon that is being buried under the mat doesn’t appear to reflect the microbes in its isotopic composition, but rather comprises the organisms that live in the water far above the lake floor, which cycle carbon differently and impart different isotopic signatures. As shown by Dr. Grim’s work, microbes that seem as if they would thrive in contrasting environments can coexist harmoniously, further complicating the biological record of the oceans.
It’s exactly these sorts of realizations that make analogue systems like Middle Island Sinkhole so important to study. While they may not be perfect replicas of our Earth a billion years ago, they’re about as close as we can get in available natural environments. Labs and their tightly-controlled experiments are essential for learning more about smaller-scale environments like cell structures and reaction mechanisms, but capturing the complexity of natural ecosystems is nearly impossible in a laboratory setting. The collaborative team is interested in how the microbial community responds to seasons and how carbon burial may change in this system as Michigan’s climate changes. Previous work has shown that human-induced global warming has altered carbon cycling and productivity in the Great Lakes. Studying lakes’ carbon cycling in detail, as Rico et al. have done, is critical to understanding how productivity might continue to respond to climate change.
The implications of these findings are far-reaching, but perhaps not surprising: what we see in the rock record isn’t always showing us the full story. Scientists who use these redox-sensitive elements as indicators of atmospheric oxygen (or lack thereof) should be cautious in interpreting these signatures in the rock record; just because there’s a chemical indication of low oxygen in one spot doesn’t mean that oxygen was absent everywhere. Furthermore, microbial communities that we think may be straightforward can be very flexible in how they behave. In a topic as hotly-debated as the evolution of our atmosphere and life on Earth, cautious approaches like this are necessary. The better we understand the coincidental changes in the atmosphere and biosphere and the conditions in which life evolved on our planet, the better we can know what to look for in our search for signs of extraterrestrial life. If we discover evidence that redox-sensitive elements like the ones studied here have been mobilized on the surface of another planet, we will need to know how to interpret them – and if this work has shown anything, it’s that there’s more than one way to read the rocks.
*Complete list of researchers on the sinkhole team:
Katy Rico (UM for this work; currently at McGill), Nathan Sheldon (UM), Rose Cory (UM), Greg Dick (UM), Sharon Grim (UM), Judith Klatt (UM; currently at Max Planck Institute, MPI), Anthony Chappaz (CMU), Bopi Biddanda (Grand Valley State), Lauren Kinsman-Costello (Kent State), Greg Druschel (IUPUI), Maya Gomes (Johns Hopkins), Wiebke Ziebis (University of Southern California), Arjun Chennu (MPI), and Dirk de Beer (MPI)