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Oxidative modification of LHC II associated with photosystem II and PS I-LHC I-LHC II membranes

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Abstract

Under aerobic conditions the production of Reactive Oxygen Species (ROS) by electron transport chains is unavoidable, and occurs in both autotrophic and heterotrophic organisms. In photosynthetic organisms both Photosystem II (PS II) and Photosystem I (PS I), in addition to the cytochrome b6/f complex, are demonstrated sources of ROS. All of these membrane protein complexes exhibit oxidative damage when isolated from field-grown plant material. An additional possible source of ROS in PS I and PS II is the distal, chlorophyll-containing light-harvesting array LHC II, which is present in both photosystems. These serve as possible sources of 1O2 produced by the interaction of 3O2 with 3chl* produced by intersystem crossing. We have hypothesized that amino acid residues close to the sites of ROS generation will be more susceptible to oxidative modification than distant residues. In this study, we have identified oxidized amino acid residues in a subset of the spinach LHC II proteins (Lhcb1 and Lhcb2) that were associated with either PS II membranes (i.e. BBYs) or PS I-LHC I-LHC II membranes, both of which were isolated from field-grown spinach. We identified oxidatively modified residues by high-resolution tandem mass spectrometry. Interestingly, two different patterns of oxidative modification were evident for the Lhcb1 and Lhcb2 proteins from these different sources. In the LHC II associated with PS II membranes, oxidized residues were identified to be located on the stromal surface of Lhcb1 and, to a much lesser extent, Lhcb2. Relatively few oxidized residues were identified as buried in the hydrophobic core of these proteins. The LHC II associated with PS I-LHC I-LHC II membranes, however, exhibited fewer surface-oxidized residues but, rather a large number of oxidative modifications buried in the hydrophobic core regions of both Lhcb1 and Lhcb2, adjacent to the chlorophyll prosthetic groups. These results appear to indicate that ROS, specifically 1O2, can modify the Lhcb proteins associated with both photosystems and that the LHC II associated with PS II membranes represent a different population from the LHC II associated with PS I-LHC I-LHC II membranes.

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Notes

  1. Considering only one Lhcb1 and one Lhcb2 within the trimer.

  2. For a very approximate estimate, consider an LHC II trimer which is not associated with a reaction center (for instance if it were moving between PS II and PS I during State 1 to State 2 transitions). Since each chl absorbs about 10 photons/sec (at 1800 μmoles photons/m2/sec) (Blankenship 2002) and each LHC II trimer contains 42 chl, each LHC II trimer absorbs about 420 photons/sec. If an LHC II trimer has a ½ life of 10 h, it would absorb 1.5 × 107 photons. Assuming the 3chl*-quenching mechanisms (carotenoids, NPQ and LHC II aggregation, etc.) were 99.99% effective at quenching 3chl* and that 10% of the unquenched 3chl* formed 1O2, then ~ 150 1O2 could be formed over the lifetime of the LHC II. LHC II trimers connected to reaction centers would be predicted to produce significantly less 1O2.

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Acknowledgements

This work was solely supported by the United States Department of Energy, Office of Basic Energy Sciences grant DE-FG02-09ER20310 to TMB and LKF.

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  1. Ravindra S. Kale and Jacob L. Seep have contributed equally to this work.

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  1. Department of Biological Sciences, Biochemistry and Molecular Biology Section, Louisiana State University, Baton Rouge, LA, 70803, USA

    Ravindra S. Kale, Jacob L. Seep, Laurie K. Frankel & Terry M. Bricker

  2. The Rieveschl Laboratories for Mass Spectrometry, Department of Chemistry, University of Cincinnati, Cincinnati, OH, 45221, USA

    Larry Sallans

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Kale, R.S., Seep, J.L., Sallans, L. et al. Oxidative modification of LHC II associated with photosystem II and PS I-LHC I-LHC II membranes. Photosynth Res 152, 261–274 (2022). https://doi.org/10.1007/s11120-022-00902-1

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