Adaptation of plant photosynthetic metabolism to extreme CO2 levels in Yellowstone revealed by in vivo fluorescence dynamics.

INTRODUCTION: While CO2 enrichment studies have provided valuable insights into how plants respond to elevated CO2 levels expected under future climate conditions (up to ~700 ppm), if and how photosynthesis can adapt to more extreme CO2 levels in nature remains yet unknown. Here, we investigate changes in photosynthetic metabolism in a C3 plant growing near high CO2 emission sources in Yellowstone National Park, at levels up to 6000 ppm CO2. METHODS: We analyze chlorophyll variable fluorescence emission kinetics to identify changes in the photosynthetic electron transport chain (PETC) between plants adapted to high CO2 versus control plants growing at ambient CO2. By applying short flashes using the Fast Repetition Rate Fluorometry (FRRF) technique we separate photochemical from non-photochemical quenching events. This enables monitoring electron transport from water oxidation within PSII into the downstream carrier pools (Plastoquinone (PQ), Ferrodoxin, and NADP+) of the PETC and into CO2 carboxylation within the Calvin Benson-Bassham (CBB) cycle. RESULTS: We find that plants growing near the extreme CO2 sources in Yellowstone are much slower to overcome bottlenecks in the PETC and reach lower photochemical Fv/Fm values indicative of lower photosynthetic efficiency. We observe that these plants require higher CO2 levels to activate the reactions in the CBB cycle. DISCUSSION: We conclude that plants growing near high CO2 sources are metabolically poised in Cyclic Electron Flow (CEF) at ambient CO2 concentrations and switch to Linear Electron Flow (LEF) only in high CO2. Second, after a brief period of dark time (3-4 minutes), the near-source plants more rapidly restore the PETC bottlenecks, slowing LEF and recovering CEF. This outcome retains electrons in the PQH2 pool slowing flux into the NADP+ pool through LEF and blocking utilization of CO2 by reactions in the CBB cycle. We explain this adaptive response as a coping mechanism against acidification at high CO2 growth conditions, which compromises enzymatic activity and proton motive force generation. We conclude that plants adapt to extreme atmospheric CO2 by further compromising the inefficient CBB cycle and by rerouting electron flux through the PETC from LEF into CEF to stimulate more proton pumping and ATP production.