Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility

Abstract

Paracoccus denitrificans and its near relative Paracoccus versutus (formerly known as Thiobacilllus versutus) have been attracting increasing attention because the aerobic respiratory system of P. denitrificans has long been regarded as a model for that of the mitochondrion, with which there are many components (e.g., cytochrome aa3 oxidase) in common. Members of the genus exhibit a great range of metabolic flexibility, particularly with respect to processes involving respiration. Prominent examples of flexibility are the use in denitrification of nitrate, nitrite, nitrous oxide, and nitric oxide as alternative electron acceptors to oxygen and the ability to use C1 compounds (e.g., methanol and methylamine) as electron donors to the respiratory chains. The proteins required for these respiratory processes are not constitutive, and the underlying complex regulatory systems that regulate their expression are beginning to be unraveled. There has been uncertainty about whether transcription in a member of the alpha-3 Proteobacteria such as P. denitrificans involves a conventional sigma70-type RNA polymerase, especially since canonical -35 and -10 DNA binding sites have not been readily identified. In this review, we argue that many genes, in particular those encoding constitutive proteins, may be under the control of a sigma70 RNA polymerase very closely related to that of Rhodobacter capsulatus. While the main focus is on the structure and regulation of genes coding for products involved in respiratory processes in Paracoccus, the current state of knowledge of the components of such respiratory pathways, and their biogenesis, is also reviewed.

FIG. 1

Branched electron transport chains of Paracoccus species. Enzyme complexes colored black indicate a periplasmic location. Electron transfer between cytochromes c₅₅₂ and c₅₅₀ has not been demonstrated experimentally but is possible, given the redox potential of the proteins. The exact nature of the roles of cytochrome c₅₅₀ and pseudoazurin is currently being studied. UQ = ubiquinone, UQH₂ = reduced ubiquinone. TOMES, thiosulfate oxidation multienzyme system.

FIG. 2

Branched electron transport pathway of P. denitrificans under various conditions of oxygen limitation. FeS, iron-sulfur center; NDH, NADH-ubiquinone oxidoreductase; SDH, succinate dehydrogenase; Q, ubiquinone pool.

FIG. 3

Denitrification pathway of P. denitrificans, with succinate as the carbon and energy source. FeS, iron-sulfur center; NDH, NADH-ubiquinone oxidoreductase; SDH, succinate dehydrogenase; Nar, nitrate reductase; Nor, nitric oxide reductase; Nir, nitrite reductase; Nos, nitrous oxide reductase; Q, ubiquinone pool; ?, unknown transporter. The exact electron pathway(s) through the c-type cytochromes and pseudoazurin is not known.

FIG. 4

Denitrification gene clusters of Pseudomonas stutzeri (A), Pseudomonas aeruginosa (B), and P. denitrificans Pd1222 (C). Reproduced with permission from reference .

FIG. 5

Electron transport pathway of P. denitrificans during growth on methylamine and methanol. FyDH, formaldehyde dehydrogenase; FoDH, formate dehydrogenase; FeS, iron-sulfur center; NDH, NADH-ubiquinone oxidoreductase; GSH, glutathione. The exact electron pathway(s) through the c-type cytochromes is not known.

FIG. 6

Regulation of gene expression during C₁ metabolism in P. denitrificans. P, promoter; FyDH, formaldehyde dehydrogenase; XDH, xox gene products; Ami, amicyanin; SS, unknown signal sensor; RR, unknown response regulator; 2CR, two-component regulatory genes.

FIG. 7

Thiosulfate-oxidizing multienzyme system. The figure is derived from the scheme devised by Kelly (140) for P. versutus. SCO, sulfite:cytochrome c oxidoreductase; A, enzyme A (SoxA); B, enzyme B (SoxB).

FIG. 8

Comparison of TyrR-dependent promoters in E. coli (Ec) and S. typhimurium (St) with the tyrB promoter region of P. denitrificans (Pd). The number at the end of the sequence denotes the percent identity of the TyrR box to the TyrR consensus.