Bacterial respiration: a flexible process for a changing environment.

The respiration of oxygen is fundamental to the life of higher animals and plants. The basic respiratory process in the mitochondria of these organisms involves the donation of electrons by low-redox-potential electron donors such as NADH. This is followed by electron transfer through a range of redox cofactors, bound to integral membrane or membrane-associated protein complexes. The process terminates in the reduction of the high-redox-potential electron acceptor, oxygen (Fig. 1). The free energy released during this electrontransfer process is used to drive the translocation of protons across the mitochondrial membrane to generate a trans-membrane proton electrochemical gradient or protonmotive force (∆p) that can drive the synthesis of ATP (Fig. 1). The respiratory flexibility of the mammalian mitochondrion is rather poor. There is some flexibility at the level of electron input (Fig. 1), but none at the level of electron output where cytochrome aa $ oxidase provides the only means of oxygen reduction. In the case of plant mitochondria, a slightly greater degree of respiratory flexibility is encountered with a number of alternative NADH dehydrogenases and two oxidases being apparent. This respiratory flexibility affords plant mitochondria with the capacity to contribute to processes other than the generation of ATP. For example, electron transfer from the alternative NADH dehydrogenase to the alternative oxidase is not coupled to the generation of ∆p and instead serves to release energy as heat, which can volatilize insect attractants to aid pollination. In the American skunk cabbage this same mechanism for heat production serves to permit growth at subzero temperatures (Nicholls & Ferguson, 1992). There is also some respiratory flexibility in the mitochondria of yeast, filamentous fungi and ancient protozoa, but it is amongst the Bacteria and Archaea that respiratory flexibility can be found at its most extreme. In these organisms, a diverse range of electron acceptors can be utilized including elemental sulphur and sulphur oxyanions (Hamilton, 1998), organic sulphoxides and sulphonates (Lie et al., 1999; McAlpine et al., 1998), nitrogen oxy-anions and nitrogen oxides (Berks et al., 1995), organic N-oxides (Czjzek et al., 1998), halogenated organics (Dolfing, 1990; Louie & Mohn, 1999; van de Pas et al., 1999), metalloid oxy-anions such as selenate and arsenate (Krafft & Macy, 1998; Macy et al., 1996, 1993; Schroder et al., 1997), transition metals such as Fe(III) and Mn(IV) (Lovley, 1991), and radionuclides such as U(VI) (Lovley & Phillips, 1992) and Tc(VII) (Lloyd et al., 1999). This respiratory diversity can be found amongst pyschrophiles, mesophiles and hyperthermophiles and contributes to the ability of prokaryotes to colonize many of Earth’s most hostile microoxic and anoxic environments.