Molecular dynamics and structural models of the cyanobacterial NDH-1 complex

Abstract

NDH-1 is a gigantic redox-driven proton pump linked with respiration and cyclic electron flow in cyanobacterial cells. Based on experimentally resolved X-ray and cryo-EM structures of the respiratory complex I, we derive here molecular models of two isoforms of the cyanobacterial NDH-1 complex involved in redox-driven proton pumping (NDH-1L) and CO 2 -fixation (NDH-1MS). Our models show distinct structural and dynamic similarities to the core architecture of the bacterial and mammalian respiratory complex I. We identify putative plastoquinone-binding sites that are coupled by an electrostatic wire to the proton pumping elements in the membrane domain of the enzyme. Molecular simulations suggest that the NDH-1L isoform undergoes large-scale hydration changes that support proton-pumping within antiporter-like subunits, whereas the terminal subunit of the NDH-1MS isoform lacks such structural motifs. Our work provides a putative molecular blueprint for the complex I-analogue in the photosynthetic energy transduction machinery and demonstrates that general mechanistic features of the long-range proton-pumping machinery are evolutionary conserved in the complex I-superfamily.

Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

“…The structural architecture thus supports that the long-range protonation signal could be triggered by dissociation of conserved ion-pairs in the antiporter-like subunits that leads to lateral proton transfer in the proton channels by coupled conformational and hydration changes ( Fig. 4) 16,19,20 .…”

“…Instead, the electrons directly enter a chain of three iron-sulphur (FeS) centres in the ferredoxin (Fd)binding domain (Fig. 1d), similar to the recently characterised NDH-1L type photosynthetic complex I and membrane-bound hydrogenases [15][16][17][18] . The PQ-binding site is located ca.…”

“…The modular membrane domain extends up to 200 Å away from the PQ reduction site, and it comprises the antiporter-like subunits NdhA, NdhB, NdhD3, and NdhF3, as well as the smaller transmembrane (TM) subunits NdhC/E/G/L. These subunits contain a chain of buried charged residues that establish central elements of the proton-pumping machinery [11][12][13][14][15][16][17]19,20 , with the isoform-specific NdhD3 and NdhF3 subunits at the terminal end of the enzyme (Fig. 1d, see below).…”

Metalloproteins in the Biology of Heterocysts

“…The NDH-1 dehydrogenase complex is a redox-driven proton pump linked with respiration and cyclic photosynthetic electron flow around PSI in cyanobacterial cells [279,280]. This complex reduces PQ and couples the released free energy to proton pumping across the membrane to drive active transport and synthesis of ATP [271,281].…”

“…Cyanobacterial NDH-1 seems to exist in two different forms involved in respiration and cyclic photosynthetic electron flow, which are termed NDH-1 1 and NDH-1 2 [280,281]. Both forms show a global architecture that closely resembles the typical L shape of the respiratory complex I [285,286,287,288], comprising a hydrophilic domain, which harbors three [4Fe–4S] clusters for electron transfer and a PQ binding site, that is connected to a wide membrane domain [280,281]. The hydrophilic domain of both NDH-1 forms comprises subunits NdhS, NdhHIJK, and NdhO and harbors the Fe–S clusters N6a, N6b, and N2 (Table 4) [271].…”