A distinct LHCI arrangement is recruited to photosystem I in Fe-starved green algae

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 122; no. 25; p. e2500621122
• Main Authors: Liu, Helen W., Khera, Radhika, Grob, Patricia, Gallaher, Sean D., Purvine, Samuel O., Nicora, Carrie D., Lipton, Mary S., Niyogi, Krishna K., Nogales, Eva, Iwai, Masakazu, Merchant, Sabeeha S.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 24.06.2025
• Subjects: Algae; Antennas; Aquatic plants; Biological Sciences; Chlorophyta; Chlorophyta - metabolism; Coding; Cryoelectron Microscopy; Cyanobacteria; Dunaliella salina; Dunaliella tertiolecta; Ferredoxin; Flavodoxin; Iron; Iron - metabolism; Light-Harvesting Protein Complexes - chemistry; Light-Harvesting Protein Complexes - metabolism; Oxidation; Photosynthesis; Photosystem I; Photosystem I Protein Complex - metabolism; Plant Biology; Proteins; phytoplankton; structural biology; iron starvation–induced protein A (isiA); iron homeostasis; TIDI
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2500621122

SignificancePhotosynthetic proteins require a significant amount of iron (Fe)-containing cofactors to function. Multisubunit Photosystem I (PSI) encompasses half of this Fe in its three Fe4S4 centers and is a target for degradation in insufficient Fe conditions, which reduces the capacity for CO2 fixation. TIDI1 (thylakoid iron deficiency induced) is an iron starvation induced chlorophyll-binding protein found in multiple green algae including Dunaliella spp. isolated from coastal Arctic waters and hypersaline ponds. These algae are especially resilient to low Fe conditions. Using single particle cryo-EM, we show PSI from Fe-starved Dunaliella spp. has a second light-harvesting chlorophyll protein tetramer containing TIDI1, showcasing a eukaryotic strategy to maintain PSI efficiency in low iron. Iron (Fe) availability limits photosynthesis at a global scale where Fe-rich photosystem (PS) I abundance is drastically reduced in Fe-poor environments. We used single-particle cryoelectron microscopy to reveal a unique Fe starvation-dependent arrangement of light-harvesting chlorophyll (LHC) proteins where Fe starvation–induced TIDI1 is found in an additional tetramer of LHC proteins associated with PSI in Dunaliella tertiolecta and Dunaliella salina. These cosmopolitan green algae are resilient to poor Fe nutrition. TIDI1 is a distinct LHC protein that co-occurs in diverse algae with flavodoxin (an Fe-independent replacement for the Fe-containing ferredoxin). The antenna expansion in eukaryotic algae we describe here is reminiscent of the iron-starvation induced (isiA-encoding) antenna ring in cyanobacteria, which typically co-occurs with isiB, encoding flavodoxin. Our work showcases the convergent strategies that evolved after the Great Oxidation Event to maintain PSI capacity.