Revealing the Importance of Organic Matter Thermodynamics in Regulating Microbial Respiration in River Sediment

The Science

Freshwater ecosystem processes contribute significant volumes of carbon to the atmosphere through aerobic respiration. It has long been thought that the microbial metabolism underlying the transformations of organic matter into available carbon are controlled by temperature and the concentration of carbon-containing molecules. However, recent field observations have suggested that thermodynamics, or the amount of chemical energy in the system available for organic matter decomposition, plays a key role in controlling microbial metabolism within river corridors, particularly in areas where groundwater and surface water mix. Now researchers have performed controlled laboratory experiments using river sediment to test organic matter thermodynamics as a mechanism of metabolic control in these environments. They find that organic matter thermodynamics control metabolism in oxygen-rich environments in ways that depend on the concentration of nutrients and organic matter.

The Impact

This work challenges a long-held belief about processes that govern organic matter metabolism in freshwater ecosystems. It is the first study to provide direct evidence for thermodynamic regulation of organic matter metabolism under oxygen-rich conditions in a controlled laboratory setting. Improving representations of river corridors with refined mechanisms of nutrient processing could improve predictive models of local to regional to global biogeochemical cycling, and could be used to help better manage river corridor ecosystems and enable prediction of changes to the integrated Earth system.

Summary

A team of scientists from Pacific Northwest National Laboratory (PNNL) and the Environmental Molecular Sciences Laboratory (EMSL) gathered sediment from the Columbia River in areas where groundwater and surface water mix. In the laboratory, they added four different organic compounds to the sediment at one of three different concentrations. Then the researchers measured the rate of metabolism and used mass spectrometry to characterize the organic molecules that remained after incubation using an ultrahigh-resolution technique. With the molecular formulas of the observed molecules in hand, the researchers calculated the amount of energy required to oxidize these molecules as a way of capturing thermodynamic favorability for decomposition. They found that organic matter thermodynamics govern aerobic microbial metabolism when organic carbon is at low concentration. As the concentration of organic carbon increased, thermodynamic controls became less influential and nutrient availability became the key factor governing metabolic rates.

Although this study is of a single freshwater ecosystem, it provides a proof of concept that can be applied to experiments in more diverse ecosystems. It also demonstrates that thermodynamic constraints, in addition to the kinetic constraints of temperature and substrate concentration, can govern aerobic metabolism. Finally, the work proposes a new conceptual model in which organic matter thermodynamic and nutrient limitations dually control aerobic metabolism. Understanding microbial metabolism at a finer resolution, as well as from a variety of mechanistic perspectives, can help improve models of local to regional to global biogeochemical cycling and can be used to help better manage river corridor ecosystems and enable prediction of changes to the integrated Earth system.

Principal Investigator(s)

Emily Graham
Pacific Northwest National Laboratory
[email protected]

Funding

This research was supported by the Office of Biological and Environmental Research, within the U.S. Department of Energy Office of Science, as part of Subsurface Biogeochemical Research Program’s Scientific Focus Area at the Pacific Northwest National Laboratory. A portion of the research was performed at the Environmental Molecular Sciences Laboratory user facility.

References

Garayburu-Caruso, V.A. et al. “Carbon limitation leads to thermodynamic regulation of aerobic metabolism.” Environmental Science & Technology Letters 7(7), 517–524 (2020). [DOI:10.1021/acs.estlett.0c00258]