Action at a distance: The remarkable coupling of CO2 uptake to electron transfer in specialized cyanobacterial NDH-1 complexes

• 成果类型: Article
• 署名作者: Zhang, Zhifen; Zhang, Minquan; Burnap, Robert L.
• 署名单位: Oklahoma State University System; Oklahoma State University - Stillwater
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-14495
• DOI: 10.1073/pnas.2511786122
• 发表日期: 2025-09-09
• 关键词: inorganic carbon pool; synechococcus pcc7942; ethoxyzolamide inhibition; concentrating mechanisms; photosynthesis; transport; genes; roles; identification; expression

摘要

Cyanobacteria achieve highly efficient photosynthesis using a CO2-concentrating mechanism relying on specialized Type I (NDH-1) complexes. Among these, NDH-1(3) and NDH-1(4) catalyze redox-coupled hydration of CO2 to bicarbonate, supporting carbon fixation in carboxysomes. The mechanism of coupling electron transfer to CO2-hydration by these variant NDH-1 complexes remains unknown. We engineered a Synechococcus PCC7942 strain that expresses exclusively the high flux/low affinity NDH-1(4) complex, enabling the observation of the coupling of CO2 hydration to cyclic electron flow in isolation from the other NDH-1 isoforms normally present in cells. We found that inhibition of the CupB protein by the carbonic anhydrase inhibitor ethoxzolamide (EZ) suppressed CO2 uptake, slowed photosystem I rereduction, and abolished proton pumping as probed by acridine orange fluorescence. These effects were absent in strains lacking Cup proteins, confirming specificity. The results demonstrate that CO2 hydration and electron transfer through NDH-1(4) are tightly coupled via proton translocation across the thylakoid membrane. These findings provide direct evidence for the bidirectional interaction in bioenergetic coupling between the plastoquinone reduction and the CO2 uptake at the distal Zn-site over a span of similar to 150 angstrom and support a proton-removal hypothesis involving the proton transfer pathways from the Zn-site of CO2 hydration to an energetically coupled proton loading site evolutionarily repurposed from the ancestral proton pumping mechanism to enable energetic CO2 uptake.