Evolution of the acceptor side of photosystem I: ferredoxin, flavodoxin, and ferredoxin-NADP+ oxidoreductase
Phototrophs of the family Heliobacteriaceae contain the simplest known Type I reaction center (RC), consisting of a homodimeric (PshA)2 core devoid of bound cytochromes and antenna proteins. Unlike plant and cyanobacterial Photosystem I in which the FA/FB protein, PsaC, is tightly bound to P700–FX cores, the RCs of Heliobacterium modesticaldum contain two FA/FB proteins, PshBI and PshBII, which are loosely bound to P800–FX cores. These two 2[4Fe–4S] ferredoxins have been proposed to function as mobile redox proteins, reducing downstream metabolic partners much in the same manner as does [2Fe–2S] ferredoxin or flavodoxin (Fld) in PS I. Using P800–FX cores devoid of PshBI and PshBII, we show that iron–sulfur cluster FX directly reduces Fld without the involvement of FA or FB (Fld is used as a proxy for soluble redox proteins even though a gene encoding Fld is not identified in the H. modesticaldum genome). The reduction of Fld is suppressed by the addition of PshBI or PshBII, an effect explained by competition for the electron on FX. In contrast, P700–FX cores require the presence of the PsaC, and hence, the FA/FB clusters for Fld (or ferredoxin) reduction. Thus, in H. modesticaldum, the interpolypeptide FX cluster serves as the terminal bound electron acceptor. This finding implies that the homodimeric (PshA)2 cores should be capable of donating electrons to a wide variety of yet-to-be characterized soluble redox partners.