Energy trade-offs under fluctuating light govern bioenergetics and growth in Chlamydomonas reinhardtii
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Abstract
Rapidly changing light intensity is a natural challenge that photosynthetic organisms can tolerate. Regulatory mechanisms of light harvesting and alternative electron pathways are critical in dissipating and distributing energy under fluctuating light intensities (FL), but less is known about downstream metabolic regulations. Here, we compared the cellular responses of Chlamydomonas reinhardtii grown under FL to cells acclimated to constant high (HL) or low light (LL), either under high (2 %) or low (0.04 %) CO 2 . Under low CO 2 , the physiology of FL cells resembled HL cells and proteomics revealed an induction of the ATP consuming carbon-concentrating mechanism, and photorespiration particularly under FL. High CO 2 promoted growth under FL, albeit by a lesser extent than under HL and led to higher ATP contents than under low CO 2 . To fuel ATP production under low CO 2 , cells upregulated mitochondrial respiration under FL, while enhanced cyclic electron flow and redox shuttling between intracellular compartments was most evident under FL and LL. Chloroplastic carbon metabolism rapidly responded to light changes, independent of CO 2 availability, whereas metabolites associated with mitochondrial bioenergetics responded slower, and remained abundant under high CO 2 . The accumulation of enzymes involved in starch synthesis and breakdown under FL, together with the transient accumulation of hexoses and hexose phosphates, indicated that cells relied on sugars as a transient carbon pool to meet changing metabolic demands under FL. We conclude that the interplay between light intensity and CO₂ availability drives critical energy trade-offs, balancing photoprotection, repair, and carbon allocation, that regulate growth under FL.
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Energy trade-offs under fluctuating light govern bioenergetics and growth in Chlamydomonas reinhardtii
Your integration of physiology, proteomics, and metabolomics across fluctuating-light and CO₂ conditions gives a clear, comprehensive picture of how C. reinhardtii shifts its energy budget when light and carbon availability vary. Ambient CO₂ drives cells into an ATP-limited, CCM-dependent state, while elevated CO₂ produces a more energetically permissive one; chloroplast-to-mitochondria electron flow becomes the dominant ATP-support pathway under carbon limitation, more than cyclic electron flow or flavodiiron activity. This opens up a few questions:
Because dissolved CO₂ is naturally low in aquatic habitats, ambient CO₂ in the lab recreates Chlamydomonas’ typical carbon environment, but it also forces continuous CCM activity and …
Energy trade-offs under fluctuating light govern bioenergetics and growth in Chlamydomonas reinhardtii
Your integration of physiology, proteomics, and metabolomics across fluctuating-light and CO₂ conditions gives a clear, comprehensive picture of how C. reinhardtii shifts its energy budget when light and carbon availability vary. Ambient CO₂ drives cells into an ATP-limited, CCM-dependent state, while elevated CO₂ produces a more energetically permissive one; chloroplast-to-mitochondria electron flow becomes the dominant ATP-support pathway under carbon limitation, more than cyclic electron flow or flavodiiron activity. This opens up a few questions:
Because dissolved CO₂ is naturally low in aquatic habitats, ambient CO₂ in the lab recreates Chlamydomonas’ typical carbon environment, but it also forces continuous CCM activity and high ATP demand. How do you define the appropriate “baseline physiology” in this context? Should the CCM-on, low-CO₂ state be treated as the reference, or is the high-CO₂, CCM-off state a more useful baseline for interpreting metabolic and proteomic differences?
Your data also raise questions about standard Chlamydomonas culturing practices. Most labs grow cells in constant light at ambient CO₂, which your results suggest enforces a high-ATP-demand, CCM-dominated state. Do you think culturing norms should shift toward supplemented CO₂ or specific fluctuating-light regimes for baseline studies? If ambient CO₂ is the ecologically relevant state, how should we interpret findings generated under 2% CO₂, where major ATP sinks are artificially suppressed?
Lastly, given the strong mitochondrial contribution under carbon limitation, did you examine mitochondrial positioning or morphology under LL, HL, and FL conditions? It would also be useful to know whether different fluctuating-light pulse lengths shift reliance on malate-based chloroplast–mitochondria shuttling. Prior work shows CO₂-dependent mitochondrial repositioning (doi: 10.1111/tpj.70601), suggesting that both structural changes and fluctuation frequency could help distinguish productive from non-productive shuttling states.
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