How biomarkers can record and reconstruct climate trends

Nestled within sediments that accumulate in marine environments, a certain class of molecule-sized fossils (biomarkers) sneakily record surface-water temperature changes over time. For almost two decades, scientists have used these molecules, found in cell membranes of organisms and called glycerol dibiphytanyl glycerol tetraether lipids (GDGTs), to reconstruct climate trends experienced over both regional and local marine environments. These microorganisms optimize cell membrane fluidity by adjusting the chemical composition and number of cell membrane lipids collectively known as TEX86 in response to environmental temperature changes fairly reliably: Relatively more lipids with a greater number of carbon rings are thought to be produced at higher temperatures.

But a mystery remained: No one fully underderstood the mechanisms by which the complex membrane-spanning GDGTs encoded information about temperature, or which organisms actually contributed to the sedimentary GDGT signals. That's now set to change, thanks to scientists associated with the MIT Department of Earth, Atmospheric and Planetary Sciences (EAPS).

Former EAPS postdoc Paula Welander, now an associate professor of earth systems science at Stanford University, recently led an effort to understand just how GDGTs are built, as well as how that information relates to the GDGTs produced in the oceans today and, potentially, in the distant past. In a study published last month in PNAS, Welander — along with first-author Zhirui Zeng of Stanford University and colleagues from Stanford and MIT — employed a combined organic geochemical, bioinformatic, and microbiological approach to fill in the details on GDGT biosynthesis.

To start, the researchers identified a related type of archaeon, called Sulfolobus acidocaldarius, that produced GDGTs with carbon rings, much like the GDGTs produced by marine organisms. While S. acidocaldarius does not grow in marine environments, a genetically tractable archaeal system is already in place for this model organism — that is, scientists can genetically manipulate it by inserting or deleting genes and seeing how those changes affect its physiology and its membrane lipids. S. acidocaldarius is also well-characterized, and also grows quickly, enabling researchers to study their manipulations within days, rather than weeks or months. 

Within S. acidocaldarius, the researchers found three genes that might encode the ring-building mechanisms in GDGTs, and then they deleted them one by one. These mutants showed the scientists that only two of the deletions affected the resulting proteins, which influenced the number of rings present in the GDGTs. When they performed the two deletions together, the new GDGTs no longer contained rings. To further confirm the roles the two genes play in ring-building, the researchers expressed the genes in another organism that doesn’t normally produce GDGTs with rings, Methanosarcina acetivorans. Once the genes were expressed, M. acetivorans began to produce GDGTs containing carbon rings. 

To study the GDGTs produced, Welander, a microbiologist, turned to former EAPS postdoc Xiaolei Liu, now assistant professor of organic geochemistry at the University of Oklahoma, and Roger Summons, the Schlumberger Professor of Geobiology in EAPS. Liu, the world’s leading expert on identifying GDGTs by mass spectrometry, was not only able to confirm that two genes were needed to make the cyclized (ring) GDGT, but also that they operated in a sequential manner. One gene encodes a protein, which adds rings near the center of the molecule, and the second gene's produced protein adds more rings to the outer edges.

Further, the researchers analyzed the phylogenetics to pinpoint the source of these cyclized GDGTs, which is a considerable source of uncertainty with respect to their use as paleotemperature proxies.

“This was an exciting collaboration to participate in because earlier work conducted in our laboratory suggested that there may be multiple clades of archaea contributing to the TEX86 signal in the ocean,” Summons says. “The new research shows that this does not seem to be the case and that it is one clade, the marine Thaumarchaeota [not Euryarchaeota], that appears responsible, thereby improving the focus for future research directions.”

This study was funded by the Simons Foundation Collaboration on the Origins of Life, the U.S. National Science Foundation, and the U.S. Department of Energy. 

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