Saturation of thylakoid-associated fatty acids facilitates bioenergetic coupling in a marine diatom allowing for thermal acclimation

TY - JOUR

T1 - Saturation of thylakoid-associated fatty acids facilitates bioenergetic coupling in a marine diatom allowing for thermal acclimation

AU - Cheong, Kuan Yu

AU - Firlar, Emre

AU - Ficaro, Lia

AU - Gorbunov, Maxim Y.

AU - Kaelber, Jason T.

AU - Falkowski, Paul G.

N1 - Funding Information: Funding was provided by the Bennett L. Smith endowment to PGF. We thank Fatematuzzuhara Nabeela, Maeve McCarty, Anna Antal and Jordan T. Standig for scoring thylakoid ultrastructure. We are grateful to Benjamin Bailleul and Pierre Joliot for designing the ECS assays. We thank Kevin Wyman for help in laboratory analyses. Publisher Copyright: © 2021 John Wiley & Sons Ltd.

PY - 2021/7

Y1 - 2021/7

N2 - In a rapidly warming world, we ask, “What limits the potential of marine diatoms to acclimate to elevated temperatures?,” a group of ecologically successful unicellular eukaryotic photoautotrophs that evolved in a cooler ocean and are critical to marine food webs. To this end, we examined thermal tolerance mechanisms related to photosynthesis in the sequenced and transformable model diatom Phaeodactylum tricornutum. Data from transmission electron microscopy (TEM) and fatty acid methyl ester-gas chromatography mass spectrometry (FAME-GCMS) suggest that saturating thylakoid-associated fatty acids allowed rapid (on the order of hours) thermal tolerance up to 28.5°C. Beyond this critical temperature, thylakoid ultrastructure became severely perturbed. Biophysical analyses revealed that electrochemical leakage through the thylakoid membranes was extremely sensitive to elevated temperature (Q10 of 3.5). Data suggest that the loss of the proton motive force (pmf) occurred even when heat-labile photosystem II (PSII) was functioning, and saturation of thylakoid-associated fatty acids was active. Indeed, growth was inhibited when leakage of pmf through thylakoid membranes was insufficiently compensated by proton input from PSII. Our findings provide a mechanistic understanding of the importance of rapid saturation of thylakoid-associated fatty acids for ultrastructure maintenance and a generation of pmf at elevated temperatures. To the extent these experimental results apply, the ability of diatoms to generate a pmf may be a sensitive parameter for thermal sensitivity diagnosis in phytoplankton.

AB - In a rapidly warming world, we ask, “What limits the potential of marine diatoms to acclimate to elevated temperatures?,” a group of ecologically successful unicellular eukaryotic photoautotrophs that evolved in a cooler ocean and are critical to marine food webs. To this end, we examined thermal tolerance mechanisms related to photosynthesis in the sequenced and transformable model diatom Phaeodactylum tricornutum. Data from transmission electron microscopy (TEM) and fatty acid methyl ester-gas chromatography mass spectrometry (FAME-GCMS) suggest that saturating thylakoid-associated fatty acids allowed rapid (on the order of hours) thermal tolerance up to 28.5°C. Beyond this critical temperature, thylakoid ultrastructure became severely perturbed. Biophysical analyses revealed that electrochemical leakage through the thylakoid membranes was extremely sensitive to elevated temperature (Q10 of 3.5). Data suggest that the loss of the proton motive force (pmf) occurred even when heat-labile photosystem II (PSII) was functioning, and saturation of thylakoid-associated fatty acids was active. Indeed, growth was inhibited when leakage of pmf through thylakoid membranes was insufficiently compensated by proton input from PSII. Our findings provide a mechanistic understanding of the importance of rapid saturation of thylakoid-associated fatty acids for ultrastructure maintenance and a generation of pmf at elevated temperatures. To the extent these experimental results apply, the ability of diatoms to generate a pmf may be a sensitive parameter for thermal sensitivity diagnosis in phytoplankton.

KW - diatom

KW - electrochromic shift (ECS)

KW - fatty acid

KW - photosynthesis

KW - proton motive force (pmf)

KW - thermal acclimation

KW - thermal tolerance

KW - thylakoid membrane

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U2 - 10.1111/gcb.15612

DO - 10.1111/gcb.15612

M3 - Article

C2 - 33749034

SN - 1354-1013

VL - 27

SP - 3133

EP - 3144

JO - Global Change Biology

JF - Global Change Biology

IS - 13

ER -