Bd oxidase homologue of photosynthetic purple sulfur bacterium Allochromatium vinosum is co-transcribed with a nitrogen fixation related gene

Abstract

Purple sulfur bacteria, which are known to be the most ancient among anoxygenic phototrophs, play an important role in the global sulfur cycle. Allochromatium vinosum oxidizes reduced sulfur compounds such as hydrogen sulfide, elemental sulfur and thiosulfide. At low oxygen concentrations, A. vinosum can grow chemotrophically using oxygen as the terminal electron acceptor. Being also a nitrogen fixer, A. vinosum is faced with the paradox of co-existence of aerobic metabolism and nitrogen fixation. Due to growth difficulties, only a few studies have dealt with the aerobic metabolism of the organism and, until now, there has been no information about the genes involved in the respiratory metabolism of purple sulfur bacteria. In this article we show the first terminal oxidase gene for A. vinosum. The presence of a Bd type of quinol oxidase is necessary to protect nitrogenases against the inhibitory effects of oxygen. In this case, a nitrogen fixation related gene is part of the cyd operon and this gene is co-transcribed with cydAB genes. Bd oxidase of A. vinosum may be the earliest form of oxidase where the function of the enzyme is to scavenge the contaminant oxygen during nitrogen fixation. This may be an important clue about the early evolution of oxygenic photosynthesis, perhaps as a protective mechanism for nitrogen fixation.

The cytochrome bd respiratory oxygen reductases

“…Cytochrome bd facilitates both pathogenic and commensal bacteria to colonize O 2 -poor environments [86–89], serves as an O 2 scavenger to inhibit degradation of O 2 -sensitive enzymes such as nitrogenase [90–98], and support anaerobic photosynthetic growth [99]. It is of interest to note that bd -type oxygen reductases predominate in the respiratory chains of bacteria that cause such diseases as bacillary dysentery [100], brucellosis [88,101], tuberculosis [87], pneumonia, life-threatening sepsis, meningitis [102], as well as Salmonella [103,104], Bacteroides [86], and Listeria monocytogenes [105] infections.…”

Complete genome sequence of Allochromatium vinosum DSM 180T

“…Photoorganoheterotrophic growth occurs with formate, acetate, propionate, butyrate, pyruvate, fumarate, succinate, malate and glycolate as organic electron donors. At reduced oxygen partial pressure even chemoorganoheterotrophic and chemolithoautotrophic growth in the dark is possible with oxygen as the terminal electron acceptor [26]. Under such conditions A. vinosum and A. minutissimum assimilate sulfate.…”

“…Besides phototrophic growth, A. vinosum is also able to grow chemotrophically with oxygen as an electron acceptor under low oxygen concentration [26]. The genome sequence of A. vinosum reveals the presence of two oxidases working preferentially under microaerobic conditions.…”

“…Alvin_2499 and Alvin_2500 encode for a cytochrome bd oxidase that is widely distributed among Archaea and Bacteria [102]. The function of the bd oxidase is to scavenge toxic oxygen during nitrogen fixation as it was shown to be co-transcribed with a nitrogen fixation related gene that is located upstream of oxidase subunit I [26]. Furthermore, A. vinosum possesses a cytochrome cbb 3 oxidase (Alvin_0781 to Alvin_0784), a member of the heme-copper oxidase family.…”

Systematic genomic analysis reveals the complementary aerobic and anaerobic respiration capacities of the human gut microbiota

“…The first type includes cytochrome bd reductases, which have a high affinity to molecular oxygen and are usually expressed under low oxygen concentrations. In certain organisms, these reductases participate in both respiration and oxygen defense (Moshiri et al, 1991 ; Dincturk et al, 2011 ), and reductases of this type are necessary when there are micro- or nanomolar concentrations of oxygen (Baughn and Malamy, 2004 ). We deemed these reductases as “microaerobic.” The second type of reductases includes enzymes with various cytochromes (Table S2 in Supplementary Materials).…”