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Dynamic diversity of the tryptophan pathway in chlamydiae: reductive evolution and a novel operon for tryptophan recapture.

ABSTRACT: BACKGROUND:Complete genomic sequences of closely related organisms, such as the chlamydiae, afford the opportunity to assess significant strain differences against a background of many shared characteristics. The chlamydiae are ubiquitous intracellular parasites that are important pathogens of humans and other organisms. Tryptophan limitation caused by production of interferon-gamma by the host and subsequent induction of indoleamine dioxygenase is a key aspect of the host-parasite interaction. It appears that the chlamydiae have learned to recognize tryptophan depletion as a signal for developmental remodeling. The consequent non-cultivable state of persistence can be increasingly equated to chronic disease conditions. RESULTS:The genes encoding enzymes of tryptophan biosynthesis were the focal point of this study. Chlamydophila psittaci was found to possess a compact operon containing PRPP synthase, kynureninase, and genes encoding all but the first step of tryptophan biosynthesis. All but one of the genes exhibited translational coupling. Other chlamydiae (Chlamydia trachomatis, C. muridarum and Chlamydophila pneumoniae) lack genes encoding PRPP synthase, kynureninase, and either lack tryptophan-pathway genes altogether or exhibit various stages of reductive loss. The origin of the genes comprising the trp operon does not seem to have been from lateral gene transfer. CONCLUSIONS:The factors that accommodate the transition of different chlamydial species to the persistent (chronic) state of pathogenesis include marked differences in strategies deployed to obtain tryptophan from host resources. C. psittaci appears to have a novel mechanism for intercepting an early intermediate of tryptophan catabolism and recycling it back to tryptophan. In effect, a host-parasite metabolic mosaic has evolved for tryptophan recycling.

SUBMITTER: Xie G

PROVIDER: S-EPMC126876 | biostudies-literature | 2002 Aug

REPOSITORIES: biostudies-literature

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Dynamic diversity of the tryptophan pathway in chlamydiae: reductive evolution and a novel operon for tryptophan recapture.

Xie Gary G Bonner Carol A CA Jensen Roy A RA

Genome biology 20020829 9

<h4>Background</h4>Complete genomic sequences of closely related organisms, such as the chlamydiae, afford the opportunity to assess significant strain differences against a background of many shared characteristics. The chlamydiae are ubiquitous intracellular parasites that are important pathogens of humans and other organisms. Tryptophan limitation caused by production of interferon-gamma by the host and subsequent induction of indoleamine dioxygenase is a key aspect of the host-parasite inter ...[more]

PMID: 12225590

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Project description:Organohalide respiration (OHR) is a bacterial anaerobic process in which halogenated compounds, e.g. tetrachloroethene (PCE), are used as terminal electron acceptors. Our model organisms are Dehalobacter restrictus strain PER-K23, an obligate OHR bacterium, and Desulfitobacterium hafniense strain TCE1, a bacterium with a versatile energy metabolism. The key catalytic enzyme is the tetrachloroethene reductive dehalogenase (PceA) that is, at genomic level, encoded in a highly conserved gene cluster (pceABCT) in both D. restrictus and D. hafniense strain TCE1. To date, the functions of PceA and PceT, a dedicated molecular chaperone for the maturation of PceA, are well defined. However, the role of PceB and PceC are still not elucidated. Here, we present a multilevel study aiming at deciphering the stoichiometry of the pceABCT individual gene products. The investigation was assessed at RNA level by reverse transcription and (quantitative) polymerase chain reaction, while at protein level, proteomic analyses based on parallel reaction monitoring were performed to quantify the PceA, B, C and T proteins in cell-free extracts as well as in soluble and membrane fractions of both strains using heavy-labelled reference peptides. At RNA level, our results confirmed the co-transcription of all pce gene products, while the quantitative analysis revealed a relative stoichiometry of the gene transcripts of pceA, pceB, pceC and pceT at approximately 1.0:3.0:0.1:0.1 in D. restrictus. This trend was not observed in D. hafniense strain TCE1, where no substantial difference was measured for the four genes. At proteomic level, a 2:1 stoichiometry of PceA and PceB was observed in the membrane fraction, and a low abundance of PceC in comparison to the other two proteins. In the soluble fraction, a 1:1 stoichiometry of PceA and PceT was identified. In summary, we show that the pce gene cluster is transcribed as an operon with, however, a level of transcription that differs for individual genes, an observation that could be explained by post-transcriptional events, such as RNA processing and differential RNA stability. Results at protein level suggest that PceA and PceB form a membrane-bound PceA2B protein complex, which, in contrast to the proposed model, seems to be devoid of PceC.

Dataset Information

Dynamic diversity of the tryptophan pathway in chlamydiae: reductive evolution and a novel operon for tryptophan recapture.

Publications

Dynamic diversity of the tryptophan pathway in chlamydiae: reductive evolution and a novel operon for tryptophan recapture.

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