Photosynthesis at the Edge: A Unifying Bioenergetic Framework for Extreme Environments

1. Introduction:

Harsh environments do not simply suppress photosynthesis; rather, they disturb the coordination between energy input, electron transport, ATP and NADPH production, and downstream metabolic demand (D. Kramer and Evans 2010; Walker et al. 2020; Arshad et al. 2022). Organisms from extreme environments have evolved strikingly different solutions to these bioenergetic challenges. The desert alga Chlorella ohadii combines antenna reduction, thylakoid remodelling and metabolic flexibility to tolerate extreme irradiance (Treves et al. 2020, 2016, 2013), whereas the Antarctic alga Chlamydomonas priscuii relies strongly on cyclic electron flow under cold, saline and light-limited conditions (Szyszka-Mroz et al. 2019; Kalra et al. 2020; Stahl-Rommel et al. 2022). By contrast, boreal conifers use still different strategies, including sustained excitation-energy redistribution and flavodiiron-mediated O₂ (Bag et al. 2020, 2023, 2025).

Together, these examples indicate that survival in harsh environments depends not only on protecting individual photosynthetic complexes, but also on coordinating excitation energy, electron flow, ATP/NADPH production, carbon metabolism and redox homeostasis (D. Kramer and Evans 2010; Walker et al. 2020). Nevertheless, harsh-environment photosynthesis has often been organised either according to environmental stress, such as cold, heat, drought or salinity, or according to individual protective mechanisms, including cyclic electron flow (CEF) and non-photochemical quenching (NPQ) (Shikanai 2014; Aguiló-Nicolau et al. 2025). Although useful, these classifications make it difficult to identify common bioenergetic principles across unrelated organisms and environments. They can also encourage individual pathways to be considered in isolation, even though their physiological functions depend on the wider energy-balancing network and may be buffered by compensatory changes elsewhere in metabolism.

Here, I propose that diverse environmental stresses can be interpreted through defined recurring modes of photosynthetic bioenergetic imbalance: excess excitation pressure, carbon-sink limitation, ATP-demand stress, redox overload and energy limitation. Rather than being defined by habitat or by the pathway activated in response, each mode is defined by the primary energetic constraint that becomes disproportionate: excitation input, metabolic sink capacity, ATP/reductant demand, electron-acceptor capacity or usable photochemical energy supply. The modes are not mutually exclusive; one may generate another, and several may coexist within the same organism or environmental condition. Their distinction therefore lies primarily in where the imbalance originates, rather than in the downstream phenotype that eventually develops.

This work takes one step forward the existing concepts of photosynthetic energy balance (D. Kramer and Evans 2010; Walker et al. 2020). The energetic framework asks which component of the energy network becomes primarily limiting or excessive under a particular environmental condition. It therefore converts the general concept of energy balance into a set of diagnosable imbalance states that can be compared across distantly related organisms. The framework does not propose new bioenergetic mechanisms; rather, it provides a common axis along which existing and future mechanistic data can be organised, compared and experimentally tested across taxa, habitat and employed globally for applied purposes.

2. Why Extreme Environments Disrupt Chloroplast Energy Balance

During the light-dependent reactions, the photosystems capture solar energy and convert it into the chemical energy carriers ATP and NADPH (Cardona et al. 2018). These products are subsequently consumed by the Calvin cycle, which assimilates CO₂ into carbohydrates (Benson and Calvin 1950). Reduction of one CO₂ molecule requires approximately three ATP and two NADPH, corresponding to an ATP/NADPH demand ratio of about 1.5 (Walker et al. 2020). During linear electron flow (LEF), photosystem II oxidises two water molecules, releasing O₂, four electrons and four protons into the thylakoid lumen (Lubitz et al. 2008). The electrons are transferred through plastoquinone and Cytb₆f to plastocyanin and photosystem I, while the Cytb₆f Q-cycle contributes additional proton translocation (Dumas et al. 2016). The resulting proton motive force (pmf), comprising the membrane potential (Δψ) and proton concentration gradient (ΔpH), drives ATP synthesis through chloroplast ATP synthase (Burlacot 2023; Dumas et al. 2016). Depending on the proton accounting assumptions (D. M. Kramer et al. 2003; Avenson et al. 2005; Takizawa et al. 2007), LEF produces NADPH and ATP in a constrained ratio due to the higher c-ring stoichiometry of chloroplastic ATP synthase compared to other ATP synthases (D. Kramer and Evans 2010; Allen 2002). However, the energetic requirements of the chloroplast are not fixed. Photorespiration, nutrient assimilation, protein repair, ion transport, carbon-concentrating mechanisms and stress metabolism can all alter ATP and NADPH demand relative to that of the CBB cycle (Bauwe et al. 2010; Mackinder 2018; Badger and Price 2003). LEF alone may therefore be insufficient to match the changing energetic and redox requirements imposed by non-optimal environments, making alternative electron and metabolic pathways important for restoring chloroplast energy balance (Shikanai 2014; Walker et al. 2020).

Photosynthetic energy balance can therefore be considered as coordination among five coupled constraints. Type I, excess excitation pressure, represents an energy-input imbalance in which photon absorption exceeds the capacity for photochemistry and safe energy dissipation (Genty et al. 1989; Baker et al. 2007). Type II, carbon-sink limitation, represents an energy-consumption imbalance in which photochemical energy production exceeds the capacity of carbon fixation and associated metabolism to consume ATP and reducing power (Hald et al. 2008; Paul and Foyer 2001). Type III, ATP-demand stress, represents an energetic-stoichiometry imbalance in which cellular ATP requirement increases disproportionately relative to reducing-power demand (D. Kramer and Evans 2010; Alric and Johnson 2017; Shikanai and Yamamoto 2017). Type IV, redox overload, represents an electron-allocation imbalance in which electron delivery exceeds the capacity of available acceptors and redox-dissipation or export pathways (Hald et al. 2008; Sonoike 2011; Tiwari et al. 2016; Walker et al. 2020). Type V, energy limitation, represents an energy-supply imbalance in which photosynthetic energy generation becomes insufficient to support metabolic demand (Walker et al. 2020).

These modes represent dominant primary constraints rather than isolated physiological states. They can therefore overlap or develop sequentially. Carbon-sink limitation, for example, may secondarily restrict NADP⁺ regeneration and develop into PSI acceptor-side redox overload, whereas elevated ATP demand may stimulate CEF while simultaneously changing stromal redox poise. The classification is consequently based on the origin of the imbalance, even when different modes converge on similar downstream phenotypes.

3. Applying the Five-Mode Framework to Extreme Environments

3.1. Excess Excitaion Pressure - An Energy Input Problem

Excess excitation pressure occurs when photon absorption exceeds the combined capacity for productive photochemistry and safe energy dissipation. The defining feature of this mode is therefore excess excitation entering the photosynthetic system relative to its processing capacity, rather than an initial limitation in metabolic energy supply. This distinction separates Type I from Type V: in Type I, energy input is excessive relative to utilisation, whereas in Type V the usable energetic output of photosynthesis is itself insufficient.

This imbalance is particularly relevant when high irradiance coincides with restricted metabolism, as occurs in boreal conifers during winter and early spring or in the desert biocrust alga Chlorella ohadii following dew or rainfall. Under such conditions, absorbed excitation can temporarily exceed the capacity for photochemical utilisation and non-photochemical energy dissipation. Boreal conifers mitigate this imbalance through sustained excitation-energy redistribution, including direct PSII-to-PSI energy transfer (Bag et al. 2020) and phosphorylated PsbS-associated NPQ (Grebe et al. 2020) particularly when photon absorption continues while metabolic reactions are strongly kinetically constrained by low temperature. In contrast, C. ohadii must rapidly activate photosynthesis following rehydration while avoiding severe overexcitation under desert sunlight. It combines reduced antenna size, unusually photodamage-resistant PSII and a proposed contribution from PSII-associated cyclic electron flow (Treves et al. 2013; Ananyev et al. 2017; Levin et al. 2021).

These examples illustrate two complementary strategies for resolving Type I imbalance: reducing the amount of excitation delivered to vulnerable reaction centres or increasing the capacity to dissipate, redistribute or safely process absorbed energy. Such traits may therefore provide candidate design principles for engineering high-light-resilient photosynthesis in crops and algae.

3.2. Carbon Sink Limitation - An Energy Consumption Problem

Carbon-sink limitation occurs when photochemical ATP and reducing-power production continues, but carbon fixation and associated metabolism cannot consume these products at sufficient rates. The primary bottleneck is therefore metabolic utilisation. This distinguishes Type II from Type I, where the initiating problem is excessive excitation input, and from Type IV, where the primary limitation lies in electron-acceptor or redox-disposal capacity.

Carbon-sink limitation may develop during drought-induced restriction of CO₂ assimilation, low inorganic-carbon availability in polar environments, or early-spring conditions in conifers when photochemical activity recovers more rapidly than downstream metabolism. When electron transport continues while CO₂ assimilation is constrained, regeneration of NADP⁺ can decline, promoting ferredoxin over-reduction and PSI acceptor-side limitation. Sustained acceptor-side pressure increases the probability of charge recombination, ROS formation and damage to PSI acceptor-side cofactors (Sonoike 2011, 1996; Lima-Melo et al. 2019; Kono et al. 2022). Prolonged PSI acceptor-side limitation can consequently result in PSI photoinhibition and constrain subsequent photosynthetic recovery and growth (Tiwari et al. 2016). Organisms can mitigate this imbalance by activating pathways that rebalance ATP/reductant production or provide alternative electron sinks. Enhanced CEF can increase pmf without generating additional net NADPH, as observed in Chlamydomonas priscuii (Lima-Melo et al. 2019; Stahl-Rommel et al. 2022; Kalra et al. 2020). Electrons can also be diverted toward O₂ through flavodiiron proteins, as occurs in boreal conifers (Bag et al. 2023), or by H₂ reduction in anaerobic conditions (Kosourov et al. 2020), Mehler-ascorbate peroxidase or water-water cycle activity (Makino et al. 2002; Sun et al. 2021).

The distinction between Type II and Type IV is therefore primarily causal rather than phenotypic. Carbon-sink limitation begins because metabolism cannot consume ATP and reducing power rapidly enough; PSI acceptor-side over-reduction develops secondarily as NADP⁺ regeneration becomes restricted. In redox overload, by contrast, insufficient electron-acceptor capacity is itself the primary bottleneck.

3.3. ATP-Demand Stress - An Energy Stoichiometry Problem

ATP-demand stress occurs when cellular ATP requirement increases disproportionately relative to reducing-power demand (Alric and Johnson 2017). Its defining feature is therefore a stoichiometric mismatch between energetic demand and the ATP/NADPH output of photosynthetic electron transport, rather than a simple shortage of total energy or an inability to consume reducing power.

Environmental acclimation can shift cellular demand toward ATP-intensive processes such as ion homeostasis, osmotic adjustment, nutrient acquisition and protein turnover. Under these conditions, continued LEF may provide sufficient or even excessive reducing power while ATP availability remains limiting. This favours cyclic electron flow around PSI, in which electrons from reduced ferredoxin are recycled through the plastoquinone/cytochrome b₆f pathway, increasing pmf and thereby the capacity for ATP synthesis without net NADPH formation (Shikanai and Yamamoto 2017). Chloroplast-to-mitochondrial reductant exchange can further contribute to whole-cell energy balancing by relieving stromal reducing pressure while supporting mitochondrial ATP production (Burlacot 2023).

Cold-saline Antarctic algae such as Chlamydomonas priscuii provide a candidate example, because low temperature, salinity, restricted gas exchange and altered light regimes are likely to increase energetic costs associated with ion homeostasis and osmotic adjustment (Stahl-Rommel et al. 2022; Kalra et al. 2020). Hypersaline algae such as Dunaliella salina may represent a related state, because glycerol accumulation, ion balance and carbon remobilisation impose substantial metabolic costs (Ramachandran et al. 2023; Borowitzka 2013). hermoacidophilic red algae such as Galdieria sulphuraria and Cyanidioschyzon merolae may similarly experience elevated ATP requirements associated with pH homeostasis, membrane stability, metal tolerance and protein turnover (Krupnik 2023; Barbier et al. 2005; Schönknecht et al. 2013). Diazotrophic cyanobacteria provide a particularly clear ATP-demand example because nitrogenase activity imposes a large ATP burden, requiring photosynthetic metabolism to support both carbon assimilation and energetically expensive nitrogen fixation (Berman-Frank et al. 2003).

ATP-demand stress can overlap with carbon-sink limitation and redox overload, but the primary diagnostic feature is a disproportionate requirement for ATP relative to reducing power. CEF should therefore not be assigned a single physiological function across all three states. When ATP demand dominates, its contribution to pmf may primarily support energetic requirements; when PSI acceptor-side pressure dominates, the same pathway may contribute more strongly to photosynthetic control and photoprotection (Sonoike 2011; Finazzi and Johnson 2016). These functions are not mutually exclusive, and their relative importance is expected to depend on the underlying energetic constraint.

3.4. Redox-Overload Stress - An Electron Allocation Problem

Redox overload occurs when photosynthetic electron delivery exceeds the capacity of downstream acceptors, redox metabolism and export pathways to reoxidise reduced carriers. Its primary bottleneck is therefore electron-acceptor capacity, rather than insufficient metabolic consumption itself. This distinction is especially important for separating Type IV from Type II. In carbon-sink limitation, restricted CO₂ fixation or associated metabolism reduces ATP/NADPH consumption and can secondarily decrease NADP⁺ regeneration. In redox overload, by contrast, electron-acceptor or redox-disposal capacity is directly insufficient, even when carbon metabolism is not initially the principal limitation. Type IV may therefore arise during sudden illumination after darkness or anoxia, rapid low-to-high-light transitions, incomplete activation of ferredoxin-dependent metabolism, or restricted redox export from the photosynthetic compartment.

Under these conditions, PSI acceptor-side over-reduction can promote charge recombination, uncontrolled electron transfer to O₂, ROS formation and damage to PSI Fe-S centres (Sonoike 2011; Tiwari et al. 2016; Lima-Melo et al. 2019). A clear example occurs during re-illumination of dark-acclimated cyanobacteria or green algae, when PSI electron transfer can become active before NADP⁺ regeneration, CO₂ assimilation and stromal redox-dissipation pathways have fully adjusted to light. In organisms possessing flavodiiron proteins, electrons can be rapidly diverted from PSI acceptors to O₂, restoring acceptor availability and limiting PSI over-reduction (Ilík et al. 2017; Allahverdiyeva et al. 2015; Burlacot et al. 2021; Bag et al. 2023). PTOX-mediated oxidation of the plastoquinone pool provides an additional route for limiting over-reduction further upstream in the electron-transport chain (Krieger-Liszkay and Feilke 2016; Saroussi et al. 2019; Shirao et al. 2013).

Thus, although Types II and IV can converge on similar PSI acceptor-side phenotypes, they ask different mechanistic questions. Type II asks whether ATP and reducing power can be consumed by metabolism; Type IV asks whether photosynthetically generated electrons have sufficient downstream acceptors or routes for safe redistribution. Identifying the primary bottleneck is therefore essential for distinguishing the two states.

3.5. Energy-Limitation Stress - An Energy Supply Problem

Energy limitation occurs when usable photosynthetic energy production is insufficient to support maintenance metabolism, carbon assimilation and growth. The defining feature is therefore insufficient photochemical supply relative to metabolic requirement, rather than excess excitation or excess electron pressure. This distinction separates Type V most clearly from Type I. The two modes represent different relationships between energy input and processing capacity. In Type I, absorbed excitation is excessive relative to the system's ability to use or dissipate it. In Type V, the photochemical output available to metabolism is itself inadequate. Importantly, absolute irradiance alone does not determine which state applies relatively low light could still generate excitation pressure if downstream metabolism were even more strongly constrained, whereas genuine energy limitation occurs when ATP and reducing-power production cannot meet energetic demand.

Energy limitation is characteristic of permanently ice-covered polar lakes, deep aquatic habitats, endolithic cyanobacteria, shaded forest understories and prolonged polar darkness. Under these conditions, adaptation can act on both sides of the energy budget. Organisms may increase energy capture and conversion through antenna remodelling, altered PSI/PSII stoichiometry or state transitions, or they may reduce energetic expenditure through lower respiratory maintenance costs, reserve mobilisation, metabolic downscaling and delayed growth (Mascoli et al. 2020; Nürnberg et al. 2018; Stahl-Rommel et al. 2022; Treves et al. 2016).

Antarctic algae such as Chlamydomonas priscuii provide a relevant example, where chronic low temperature, low irradiance, altered spectral quality and seasonal darkness may favour stable low-flux photosynthesis rather than maximal photosynthetic capacity (Szyszka-Mroz et al. 2019; Aguiló-Nicolau et al. 2025). FaRLiP cyanobacteria provide another example of adaptation to limited usable light, in which red-shifted chlorophylls d and f and remodelled photosystems allow photosynthesis under far-red light regimes that are poorly exploited by conventional chlorophyll a-based photosystems (Shen et al. 2019; Ho et al. 2017). Shade-adapted understory plants may represent a related strategy, in which enlarged antenna systems, altered PSI/PSII balance and adjustments in NDH-dependent cyclic electron flow contribute to photosynthetic performance under weak, far-red-enriched light (Sonoike 2011; Kono et al. 2022). A snapshot of the five energetic modes are provided in Table 1.

4. Outlook

The conceptual advance of the five-mode framework is to shift the classification of photosynthetic stress from external environmental drivers and individual protective mechanisms to the primary bioenergetic bottleneck that they create. This distinction allows states with similar downstream phenotypes to be separated mechanistically and provides a basis for moving from descriptive stress physiology toward experimentally diagnosable and ultimately predictive photosynthetic bioenergetics. This distinction is important because the same pathway can fulfil different physiological roles depending on the dominant energetic constraint. CEF, for example, may contribute principally to ATP/reductant rebalancing under Type III conditions but increasingly to photosynthetic control under acceptor-side pressure, while alternative electron sinks may become particularly important when electron-disposal capacity constrains the system (D. Kramer and Evans 2010; Walker et al. 2020; Shikanai 2014). Thus, pathway activity alone does not diagnose the underlying energetic problem; its physiological meaning must be interpreted within the state of the wider energy-balancing network.

A major next step will be to make the five modes experimentally diagnosable by integrating chlorophyll fluorescence, P700 spectroscopy and electrochromic-shift measurements with ATP/NADPH measurements, metabolomics and stable-isotope-based flux analysis (Bag 2026; Emwas et al. 2022; Cocuron et al. 2019). Such integration should help distinguish, for example, whether PSI acceptor-side pressure originates primarily from restricted metabolic consumption or insufficient electron-acceptor capacity, and whether enhanced CEF principally reflects elevated ATP demand or photoprotective regulation.

Extreme and stress-adapted organisms provide particularly valuable systems in which to test this framework because evolution has generated diverse solutions to recurrent bioenergetic constraints. Rather than transferring individual pathways directly into crops, a more rational strategy would first identify the energetic problem solved by a natural adaptation, quantify its consequences in the native organism, and then reconstruct the mechanism in genetically tractable systems such as Arabidopsis thaliana, Chlamydomonas reinhardtii or cyanobacterial models. Once the effects on excitation pressure, ATP/reductant balance, electron allocation and metabolic flux are established, the most robust strategies can be evaluated in crop and algal production systems.

In this way, harsh environments can serve as natural discovery platforms, model organisms as systems for mechanistic validation, and crops or industrial algae as tests of translational value. The broader value of the five-mode framework is therefore to shift harsh-environment photosynthesis from a collection of habitat- and pathway-specific adaptations toward a predictive bioenergetic framework in which the primary energetic constraint can be diagnosed, the compensatory response can be predicted, and candidate adaptations can be tested on a common mechanistic basis.