The heliobacteria are a family of strictly anaerobic, Gram-positive, photoheterotrophs in the Firmicutes. They make use of a homodimeric type I reaction center (RC) that contains similar to 20 antenna bacteriochlorophyll (BChl) g molecules, a special pair of BChl g' molecules (P-800), two 8(1)-OH-Chl a(F) molecules (A(0)), a [4Fe-4S] iron-sulfur cluster (F-x), and a carotenoid (4,4'-diaponeurosporene). It is known that in the presence of light and oxygen BChl g is converted to a species with an absorption spectrum identical to that of Chl a. Here, we show that main product of the conversion is 8(1)-OH-Chl aF. Smaller amounts of two other oxidized Chl a(F) species are also produced. In the presence of light and oxygen, the kinetics of the conversion are monophasic and temperature dependent, with an activation energy of 66 +/- 2 kJ mol(-1). In the presence of oxygen in the dark, the conversion occurs in two temperature-dependent kinetic phases: a slow phase followed by a fast phase with an activation energy of 53 +/- 1 kJ mol(-1). The loss of BChl g' occurs at the same rate as the loss of Bchl g; hence, the special pair converts at However, the loss of P-800 photooxidiation and flavodoxin reduction is not linear with the loss of BChl g. In anaerobic RCs, the charge recombination between P-800(+) and F-x(-) at 80 K is monophasic with a lifetime of 4.2 ms, but after exposure to oxygen, an additional phase with a lifetime of 0.3 ms is observed. Transient EPR data show that the line width of P-800(+) increases as BChl g is converted to Chl aF and the rate of electron transfer from A(0) to F-x, as estimated from the net polarization generated by singlet-triplet mixing during the lifetime of P(800)(+)A(0)(-), is unchanged. The transient EPR data also show that conversion of the BChl g results in increased formation of triplet states of both BChl g and Chl a(F). The nonlinear loss of P-800 photooxidiation and flavodoxin reduction, the biphasic backreaction kinetics, and the increased EPR line width of P-800(+) are all consistent with a model in which the BChl g'/BChl g' and BChl g'/Chl a(F)' special pairs are functional but the Chl a(F)'/Chl a(F)' special pair is not.