Tuning Shinkarev’s Bicycle: Separating the Parallel Cycles of Photosystem II Using Empirical Wavelet Transform

TL;DR

This paper introduces a new method to analyze oxygen production in photosynthesis, separating overlapping signals to better understand the process.

Contribution

The study introduces empirical wavelet transform (EWT) to separate overlapping oscillations in oxygen yield data, improving accuracy of photosystem II analysis.

Findings

EWT successfully resolves period-four oscillations and a distinct binary oscillation in oxygen evolution data.

Using EWT improves recovery of VZAD parameters and provides more accurate estimates of S-state distributions.

The binary oscillation aligns with semiquinone dynamics predicted from period-four fit parameters.

Abstract

The oxygen-evolving complex (OEC) of Photosystem II (PSII) catalyzes light-driven water oxidation, a process necessary to sustain Earth’s atmospheric oxygen. Oxygen yields measured during single-turnover flash sequences exhibit period-four oscillations, which form the basis of the Joliot–Kok (S-state) model. However, when the oscillations of other processes contribute to the measured oxygen yield, fitting methods can conflate these signals and distort estimates of inefficiencies and initial S-state populations. To address this, we applied the empirical wavelet transform (EWT) as a model-independent method to separate overlapping oscillators and capture damping dynamics that are not well represented in Fourier analysis. We tested this framework on polarographic flash-oxygen traces from both our Synechocystis sp. PCC 6803 thylakoid membrane preparations and archival datasets on Chlorella and isolated chloroplasts. EWT consistently resolves the expected period-four component alongside a distinct binary oscillation. Simulations suggest that fitting this isolated period-four signal recovers VZAD parameters more accurately than analysis of raw traces, yielding different estimates for S-state distributions and transition probabilities. Notably, this binary oscillation aligns closely with semiquinone dynamics predicted solely from period-four fit parameters. These findings indicate that EWT can effectively distinguish complex signals in oxygen evolution, offering a framework potentially applicable to other spectroscopic probes of the S-state cycle.

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