Rapid hydrolysis rates of thio- and phosphate esters constrain the origin of metabolism to cool, acidic to neutral environments
Sebastian A. Sanden,
Christopher J. Butch,
Stuart Bartlett,
Nathaniel Virgo,
Yasuhito Sekine,
Shawn Erin McGlynn
Affiliations
Sebastian A. Sanden
Earth Life Science Institute, Tokyo Institute of Technology, 2-12-1 I7E Ookayama, Meguro, Tokyo 152-8550, Japan; Inorganic Chemistry I, Ruhr-University Bochum, Universitaetsstrasse 150, 44801 Bochum, Germany; Corresponding author
Christopher J. Butch
Earth Life Science Institute, Tokyo Institute of Technology, 2-12-1 I7E Ookayama, Meguro, Tokyo 152-8550, Japan; Department of Biomedical Engineering, College of Engineering and Applied Sciences, Nanjing University, Nanjing 210023, China; Corresponding author
Stuart Bartlett
Earth Life Science Institute, Tokyo Institute of Technology, 2-12-1 I7E Ookayama, Meguro, Tokyo 152-8550, Japan; Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125, USA
Nathaniel Virgo
Earth Life Science Institute, Tokyo Institute of Technology, 2-12-1 I7E Ookayama, Meguro, Tokyo 152-8550, Japan
Yasuhito Sekine
Earth Life Science Institute, Tokyo Institute of Technology, 2-12-1 I7E Ookayama, Meguro, Tokyo 152-8550, Japan; Institute of Nature and Environmental Technology, Kanazawa University, Ishikawa, Japan; Planetary Plasma and Atmospheric Research Center, Tohoku University, Miyagi, Japan
Shawn Erin McGlynn
Earth Life Science Institute, Tokyo Institute of Technology, 2-12-1 I7E Ookayama, Meguro, Tokyo 152-8550, Japan; Blue Marble Space Institute of Science, Seattle, WA, USA; Biofunctional Catalyst Research Team, RIKEN Center for Sustainable Resource Science, Wako, Japan; Corresponding author
Summary: Universal to all life is a reliance on energy carriers such as adenosine triphosphate (ATP) which connect energy-releasing reactions to energy-consuming processes. While ATP is ubiquitously used today, simpler molecules such as thioesters and polyphosphates are hypothesized to be primordial energy carriers. Investigating environmental constraints on the non-enzymatic emergence of metabolism, we find that hydrolysis rates—not hydrolysis energies—differentiate phosphate esters and thioesters. At temperatures consistent with thermophilic microbes, thioesters are favored at acidic pH and phosphate esters at basic pH. Thioacids have a high stability across pH 5–10. The planetary availability of sulfur and phosphate is coincident with these calculations, with phosphate being abundant in alkaline and sulfur in acidic environments. Since both sulfur esters and phosphate esters are uniquely required in metabolism, our results point to a non-thermophilic origin of early metabolism at cool, acidic to neutral environments.
