The Biogeochemical Paradox of Redox: Rethinking our Understanding of the Redox Ladder across Aquatic and Terrestrial Ecosystems

Abstract:

The biogeochemical redox ladder of alternative electron acceptors constitutes a first principle of understanding energy and matter transformations in ecosystems. The theoretical underpinning is that electron acceptors should be reduced in a predictable sequence, provided that microbes compete for electron donors in a homogeneous environment. However, we see many lines of evidence that theory does not work as cleanly as predicted in heterogeneous, natural settings. This creates a paradox: the first principle of biogeochemical studies does not always hold up in natural settings. Furthermore, the main method of measuring the dominant redox process, redox potential (also known as E_h; defined as a measure of electron availability) is often not reproducible. To better understand this redox paradox, we explore: 1) when and where redox ladders work as predicted by theory and contrast that with environments in which the ladder does not work, 2) the need to understand a redox couple from both the electron accepting and donating process, and how increased understanding of both sides may improve redox ladder predictability, and 3) the trade-offs in understanding the redox ladder using redox potential vs. the underused redox buffering capacity. We find that the redox ladder works in highly simplified or homogeneous environments (e.g., oligotrophic lake water columns), but fails in complex soil environments or environments with hydrologic variation. We also compare multiple potential electron donors, in addition to the commonly used organic carbon, to investigate how competing electron donors may influence the dominant redox couple. Finally, we argue that simply measuring redox potential isn’t a powerful enough predictor of the dominant redox couple, but instead posit that a combination of redox potential and redox buffering capacity will give superior predictive power. Incorporating these concepts into our understanding of redox ladders in naturally heterogeneous environments will improve the predictive capacity of empirical and modeling biogeochemical studies.