How Methane-Eating Microbes Respond to Rapid Environmental Change

The Extremo Files
By Jeffrey Marlow
Dec 23, 2015 8:22 PMNov 20, 2019 3:53 AM

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By David Case, Guest Contributor

Hydrate Ridge, offshore Oregon USA, is the frequently studied marine methane seep at which the experiments took place. Visible in the image are orange bacterial mats and the broken, rocky terrain characteristic to these habitats. Various deployed transplantation and colonization experiments can be seen by their associated tags — including a marker for the overall site, 'HR 3’. The arm of the submersible is visible on the left of the image, and sampling equipment is visible in the lower right. (Image: V. Orphan, L. Levin, WHOI) Imagine a landscape on the seafloor, half a mile below sea level, where the sweep of normal marine sediment – calm, flat, expansive – is interrupted by an ecosystem of astonishing diversity. Like the nighttime view from an airplane looking down on a city’s lights, you see the unmistakable signs of life: white and orange microbial mats coat the seafloor, and crabs, mussels, clams, and fish dot the area. Bubbles of methane gas emerge, swirling upward into the overlying water. The landscape is cracked and mottled, the surrounding mud giving way to a varied and rocky topography. This is a marine methane seep, a common ecosystem along the tectonic margins of most of Earth’s continents, but one that went unseen by human eyes until the 1980s. During the last five years of my research career, marine methane seeps have captured my attention for two principle reasons. These ecosystems host a rich diversity of seafloor life, and, perhaps counterintuitively, they represent an important link between biology and Earth’s climate. About 15 years ago, the scientific community discovered that microorganisms living in marine methane seeps consume methane as a food source, thereby preventing its release into the ocean and, ultimately, the atmosphere. Without this important biological filter, nearly four times more methane would escape into the ocean/atmosphere system, further contributing to climate change. Organisms at methane seeps must contend not only with near-freezing temperatures and crushing pressures, but also with frequent landscape change caused by geological forces. Over time – estimates range from months to tens of thousands of years – seeps stop, start, and move location on the seafloor. Essentially, methane seeps “turn on” and “turn off.” With methane serving as the base carbon source for a complex, interwoven food web, biological communities must adjust as previously calm areas of the seafloor begin actively venting methane, and formerly active regions become dormant. Scientists do not yet fully grasp how biological communities handle such changes in environmental conditions; it’s an important problem, since similar scenes play out all over the world where environmental conditions can change rapidly. At what rate do species respond to changing circumstances? Are some species more sensitive than others? And how do we, as scientists, perform experiments on these systems without having to wait thousands of years for the methane switch to be flipped? A PhD is only supposed to take five years, after all. One answer, it turns out, is to swap time for space. Our new study*, published this month in mBio, has done just that. Rather than wait for geological forces to modify the seep’s underlying plumbing, we collected samples from the seafloor and transplanted them. Some samples went from an actively venting seep region to a dormant area; others experienced the opposite change. These transplant experiments simulated the activation and quiescence of a marine methane seep, allowing us to track the response and behavior of microorganisms over tractable timescales.

The transplantation experiments are depicted, in which carbonate rocks (here, gray blocks) were moved from active to dormant seep sites, and vice versa. Active seep sites are characterized by methane bubbles and dense seafloor life, including tube worms, clams, and bacterial mats. Dormant sites generally exhibit less dense animal populations, though also host distinct, endemic microbial diversity. (Image: David Case) We made two remarkable discoveries. First, we found that marine methane seeps host even more diverse microbial populations than previously realized, due largely to the revelation that different microbial species populate rocks than populate the surrounding muddy sediments. Sediments have historically received the bulk of scientific attention (in part because it’s easier to scoop up mud than recover and analyze large rocks from the seafloor), but it turns out that rocks make up the vast majority of the available habitat in methane seep ecosystems. The microbes inhabiting rocks in seep settings are not only different than our traditional interpretation of seep microbiology, but they also happen to be the volumetrically dominant fraction of life in these habitats. Our second discovery came from our novel transplantation experiments, using space as a substitute for time. We found that in general, microbial communities are recalcitrant to seep quiescence (they don’t die right away when the methane supply is “turned off”) but responsive to seep activation (they change quickly when methane supply is “turned on”). These findings have major ecological implications: as conditions become less favorable, methane-fueled microbial communities may be well-adapted to wait for a return to better times. On the other hand, if seep activity is dialed up, these same organisms may be able respond quickly to consume the extra supply. This is all consistent with species evolved and adapted to live in a temporally variable environment. It’s also good news given the rapidly changing environmental conditions caused by climate change: seep microbes – the base of the food chain in these seafloor biodiversity hot spots – appear to be resilient to change on short timescales. Our observations show that given enough time under altered conditions, microbial communities do eventually succumb to the change, but it remains unclear exactly how long this transition takes. Marine methane seeps, like their more photogenic “black smoker” cousins, host a rich diversity of marine life. On average, scientists have discovered a new species living in seep and vent sites every two weeks for the last 40 years, and estimates suggest that we have explored just 20% of the worldwide habitats. The deep sea remains Earth’s most enigmatic frontier, a hidden world with global implications.

*****

*The new article in mBio by David Case, Alexis Pasulka, Jeffrey Marlow, Benjamin Grupe, Lisa Levin, and Victoria Orphan, is freely available to the public here

. David Case is a PhD candidate in Geochemistry at the California Institute of Technology. His work has focused on the impact of environmental change on microbial communities, funded by the National Science Foundation, the NASA Astrobiology Institute, and the Gordon and Betty Moore Foundation’s Marine Microbiology Initiative. David is from Madison, WI, and he currently lives in Pasadena, CA.

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