.2024 Jul 10;75(13):4005-4023.

doi: 10.1093/jxb/erae170.

Unique photosynthetic strategies employed by closely related Breviolum minutum strains under rapid short-term cumulative heat stress

Pranali Deore¹, Sarah Jane Tsang Min Ching¹, Matthew R Nitschke^{2 3}, David Rudd⁴, Douglas R Brumley⁵, Elizabeth Hinde⁶, Linda L Blackall¹, Madeleine J H van Oppen^{1 2}

Affiliations

¹ School of BioSciences, The University of Melbourne, Parkville 3010, Victoria, Australia.
² Australian Institute of Marine Science, Townsville 4810, Queensland, Australia.
³ School of Biological Sciences, Victoria University of Wellington, Wellington 6102, New Zealand.
⁴ Drug Delivery, Disposition and Dynamics, Monash Institute of Pharmaceutical Sciences, Monash University, Parkville, VIC 3052, Australia.
⁵ School of Mathematics and Statistics, The University of Melbourne, Parkville 3010, Victoria, Australia.
⁶ School of Physics, The University of Melbourne, Parkville 3010, Victoria, Australia.

PMID:38636949
PMCID: PMC11233414
DOI: 10.1093/jxb/erae170

Unique photosynthetic strategies employed by closely related Breviolum minutum strains under rapid short-term cumulative heat stress

Pranali Deore et al. J Exp Bot.2024.

.2024 Jul 10;75(13):4005-4023.

doi: 10.1093/jxb/erae170.

Authors

Pranali Deore¹, Sarah Jane Tsang Min Ching¹, Matthew R Nitschke^{2 3}, David Rudd⁴, Douglas R Brumley⁵, Elizabeth Hinde⁶, Linda L Blackall¹, Madeleine J H van Oppen^{1 2}

Affiliations

¹ School of BioSciences, The University of Melbourne, Parkville 3010, Victoria, Australia.
² Australian Institute of Marine Science, Townsville 4810, Queensland, Australia.
³ School of Biological Sciences, Victoria University of Wellington, Wellington 6102, New Zealand.
⁴ Drug Delivery, Disposition and Dynamics, Monash Institute of Pharmaceutical Sciences, Monash University, Parkville, VIC 3052, Australia.
⁵ School of Mathematics and Statistics, The University of Melbourne, Parkville 3010, Victoria, Australia.
⁶ School of Physics, The University of Melbourne, Parkville 3010, Victoria, Australia.

PMID:38636949
PMCID: PMC11233414
DOI: 10.1093/jxb/erae170

Abstract

The thermal tolerance of symbiodiniacean photo-endosymbionts largely underpins the thermal bleaching resilience of their cnidarian hosts such as corals and the coral model Exaiptasia diaphana. While variation in thermal tolerance between species is well documented, variation between conspecific strains is understudied. We compared the thermal tolerance of three closely related strains of Breviolum minutum represented by two internal transcribed spacer region 2 profiles (one strain B1-B1o-B1g-B1p and the other two strains B1-B1a-B1b-B1g) and differences in photochemical and non-photochemical quenching, de-epoxidation state of photopigments, and accumulation of reactive oxygen species under rapid short-term cumulative temperature stress (26-40 °C). We found that B. minutum strains employ distinct photoprotective strategies, resulting in different upper thermal tolerances. We provide evidence for previously unknown interdependencies between thermal tolerance traits and photoprotective mechanisms that include a delicate balancing of excitation energy and its dissipation through fast relaxing and state transition components of non-photochemical quenching. The more thermally tolerant B. minutum strain (B1-B1o-B1g-B1p) exhibited an enhanced de-epoxidation that is strongly linked to the thylakoid membrane melting point and possibly membrane rigidification minimizing oxidative damage. This study provides an in-depth understanding of photoprotective mechanisms underpinning thermal tolerance in closely related strains of B. minutum.

Keywords: Climate change; Symbiodiniaceae; intra-specific variation; non-photochemical quenching; photoprotection; thermal tolerance.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

**Fig. 1.**
Characterization ofBreviolum minutum strains. (A) ITS2 profiles of endosymbiont communities ofExaiptasia diaphana (genotypes AIMS2 and AIMS3, abbreviated as A2 and A3; letters A–I indicate different clones). (B) Cultured monoclonal isolates: SCF-127, ITS2 profile: B1–B1o–B1g–B1p; and A2-6, A3-S12, ITS2 profile: B1–B1a–B1b–B1g. (C) Mean cell diameter (µm) of monoclonal isolates. Cell numbers (n) for cell diameter estimations were 55, 49, and 66 for SCF-127, A2-6, and A3-S12, respectively. Coloured squares represent different ITS2 profiles and bars in (A, B) and are arranged based on relative abundance. **P=0.0011, where level of significance is 0.05.

**Fig. 2.**
The thermal melting point of thylakoid membrane in threeB. minutum strains. SCF-127 has the ITS2 profile B1–B1o–B1g–B1p, and A2-6 and A3-S12 are B1–B1a–B1b–B1g. Data points indicate estimated melting temperatures of thylakoid membranes based on Weibull’s equation using maximum photosynthetic yield of photosystem II (F_v/F_m) under rapid short-term cumulative temperature stress. ****P<0.0001 where the level of significance was 0.05 (n=3 per strain).

**Fig. 3.**
Changes in photosynthetic parameters of photosystem II in the threeB. minutum strains as a function of rapid short-term cumulative temperature stress (26–40 °C). (A) Principal component analysis (bi-plot) of various photosynthetic parameters associated withB. minutum strains exposed to increasing temperatures (coloured scale). Dashed ellipses and circle indicate grouping of strains and extreme temperature (40 °C) along PC1. (B–E) Differences in photochemical δF/F_mʹ (B) and 1−qL (C) and non-photochemical Y(NPQ) (D) and Y(NO) (E) coefficients. Temperature values in (B–D) are the thylakoid membrane thermal melting points of theB. minutum strains. Data points are means ±SD,n=3 per strain.

**Fig. 4.**
Activation of photoprotection response in three strains ofB. minutum. Photoprotective response comprised of Stern–Volmer non-photochemical quenching (NPQ_SV), reactive oxygen species (ROS, cell⁻¹) and de-epoxidation state (DES) in threeB. minutum strains, SCF-127 (A), A2-6 (B), and A3-S12 (C), as a function of rapid short-term cumulative heat stress (26–40 °C). Vertical dashed lines are the thermal melting point of the thylakoid membranes for eachB. minutum strain. The bottom and top halves of they-axis show ROS and NPQ_SV datasets. The righty-axis shows DES, which is a ratio of diatoxanthin to diadinoxanthin pigments. Values on bothy-axes are arbitrary units. Data points are means ±SD,n=3 per strain.

**Fig. 5.**
Dynamic resolution of components of NPQ in threeB. minutum strains. (A) qE type or fast relaxing; (B) qI or slow relaxing; (C) qT₁; and (D) qT₂ type. Temperature values in the legend above graphs are the thermal melting points of thylakoid membranes for eachB. minutum strain. Data points are means ±SD,n=3 per strain.

**Fig. 6.**
Dynamic resolution of components of NPQ in presence of metabolic inhibitors in threeB. minutum strains. qE type or fast resolving (A), qI or slow relaxing (B), qT₁ type (C) and qT₂ type (D) components of NPQ in the presence of inhibitors ammonium chloride (NH₄Cl, 5 mM), dithiothreitol (DTT, 1 µM) and diphenyleneiodonium chloride (DPI, 1 µM). Control indicates untreated cultures and data points inside violin shaped features are values for each replicate; thick dashed line is median and thin dashes are minimum and maximum;n=3 per strain. Asterisks *, **, and *** indicateP value<0.0032, 0.0021, and 0.0002, respectively.

**Fig. 7.**
Photoprotective mechanisms employed by the three closely related strains ofB. minutum. SCF-127 (ITS2 profile B1–B1o–B1g–B1p, thylakoid melting point 35.37 °C) primarily dissipates energy through the super-quenching state (qT₂) and unregulated pathway Y(NO). SCF-127 also maintains a higher level of membrane rigidity possibly by embedding more diatoxanthin (de-epoxidase from diadinoxanthin) into the thylakoid lipid bilayer. The other strains, A2-6 and A3-S12 (ITS2 profile B1–B1a–B1b–B1g, thylakoid melting points 33.99 and 34.02 °C, respectively), predominantly dissipate heat through the fast relaxing mechanism (qE) possibly mediated by a quenching complex that contains minimal levels of diatoxanthin. Differences in the number of heat dissipation (red), diadinoxanthin (blue dumbbell) and diatoxanthin (purple dumbbell) symbols indicate relative differences in the magnitude of photoprotective processes amongB. minutum strains.

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Unique photosynthetic strategies employed by closely related Breviolum minutum strains under rapid short-term cumulative heat stress

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Unique photosynthetic strategies employed by closely related Breviolum minutum strains under rapid short-term cumulative heat stress

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Abstract

Conflict of interest statement

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