Glucose metabolism by agents of the psittacosis-trachoma group

Weiss, Emilio; Myers, William F.; Dressler, Harry R.; Chun-Hoon, H.

doi:10.1016/0042-6822(64)90076-5

Cited by 28 publications

(38 citation statements)

References 16 publications

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“…While it was initially proposed that the latter can metabolize D-glucose under host-free conditions, as inferred from the production of 14 CO 2 from 14 C-labeled D-glucose [74], [75], it was subsequently shown that the starting point for sugar catabolism in these bacteria is D-glucose-6-phosphate [65]. Moreover, experiments with substrates labeled at various carbon atoms revealed a combined action of glycolysis and PPP, yet complete TCA cycle activity could not be demonstrated [66], [74], [75]. In addition, anabolic reactions such as lipid and folate synthesis were detected in host-free Chlamydiaceae [76]–[79].…”

Section: Discussionmentioning

confidence: 99%

Metabolic Features of Protochlamydia amoebophila Elementary Bodies – A Link between Activity and Infectivity in Chlamydiae

et al. 2013

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The Chlamydiae are a highly successful group of obligate intracellular bacteria, whose members are remarkably diverse, ranging from major pathogens of humans and animals to symbionts of ubiquitous protozoa. While their infective developmental stage, the elementary body (EB), has long been accepted to be completely metabolically inert, it has recently been shown to sustain some activities, including uptake of amino acids and protein biosynthesis. In the current study, we performed an in-depth characterization of the metabolic capabilities of EBs of the amoeba symbiont Protochlamydia amoebophila. A combined metabolomics approach, including fluorescence microscopy-based assays, isotope-ratio mass spectrometry (IRMS), ion cyclotron resonance Fourier transform mass spectrometry (ICR/FT-MS), and ultra-performance liquid chromatography mass spectrometry (UPLC-MS) was conducted, with a particular focus on the central carbon metabolism. In addition, the effect of nutrient deprivation on chlamydial infectivity was analyzed. Our investigations revealed that host-free P. amoebophila EBs maintain respiratory activity and metabolize D-glucose, including substrate uptake as well as host-free synthesis of labeled metabolites and release of labeled CO2 from 13C-labeled D-glucose. The pentose phosphate pathway was identified as major route of D-glucose catabolism and host-independent activity of the tricarboxylic acid (TCA) cycle was observed. Our data strongly suggest anabolic reactions in P. amoebophila EBs and demonstrate that under the applied conditions D-glucose availability is essential to sustain metabolic activity. Replacement of this substrate by L-glucose, a non-metabolizable sugar, led to a rapid decline in the number of infectious particles. Likewise, infectivity of Chlamydia trachomatis, a major human pathogen, also declined more rapidly in the absence of nutrients. Collectively, these findings demonstrate that D-glucose is utilized by P. amoebophila EBs and provide evidence that metabolic activity in the extracellular stage of chlamydiae is of major biological relevance as it is a critical factor affecting maintenance of infectivity.

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Section: Discussionmentioning

confidence: 99%

Metabolic Features of Protochlamydia amoebophila Elementary Bodies – A Link between Activity and Infectivity in Chlamydiae

et al. 2013

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“…Although most of the studies on carbohydrate metabolism in the psittaco sis group have been done with the agents of meningopneumonitis and trachoma, five other organisms have also been studied (53,128). All metab olized glucose in essentially the same manner, but there were minor and, as yet, imperfectly understood differences.…”

Section: Energy Metabolismmentioning

confidence: 98%

“…The validity of this concept was questioned when Weiss and his associates (128) found that purified preparations of six different members of the group degraded MOULDER C14-labeled glucose with the liberation of CO2 from the C1 and C3•4, but not C6, positions. Comparable preparations from uninfected host tissues were without such activity.…”

Section: Energy Metabolismmentioning

confidence: 98%

The Relation of the Psittacosis Group (Chlamydiae) to Bacteria and Viruses

Moulder¹

1966

Annu. Rev. Microbiol.

115

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“…By studying bacteria that were grown and subsequently purified from embryonated chicken eggs, Weiss et al could demonstrate that C. trachomatis and C. psittaci were capable of utilizing D-glucose, as inferred from the observed release of radioactive CO 2 from 14 C-labeled D-glucose (Ormsbee & Weiss, 1963;Weiss et al, 1964). However, this substrate did not stimulate increased oxygen consumption and while production of labeled CO 2 was readily observed in the presence of D-glucose labeled at either carbon atom 1, or carbon atoms 3 and 4, or randomly, liberation of carbon 6 could not be observed (Ormsbee & Weiss, 1963;Weiss et al, 1964).…”

Section: The Pregenomic Eramentioning

confidence: 99%

“…Despite the apparent lack of a complete TCA cycle or aerobic respiration, activity of the glycolytic pathway could be demonstrated in host-free Chlamydia spp., based on the observation that isotopically labeled pyruvate could be formed from D-glucose even when this substrate was labeled only at position 1, a carbon atom that would have been released as CO 2 earlier if the pyruvate would have been formed solely via the alternative pentose phosphate pathway (Weiss et al, 1964). Interestingly, although glycolytic activity should enable the bacteria to produce a certain amount of ATP by substrate-level phosphorylation, utilization of D-glucose by Chlamydia spp.…”

Section: The Pregenomic Eramentioning

confidence: 99%

Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities

Omsland¹,

Sixt²,

et al. 2014

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Chlamydiae are a group of obligate intracellular bacteria comprising important human and animal pathogens as well as symbionts of ubiquitous protists. They are characterized by a developmental cycle including two main morphologically and physiologically distinct stages, the replicating reticulate body and the infectious non-dividing elementary body. In this review we reconstruct the history of studies that have led to our current perception of chlamydial physiology, focusing on their energy and central carbon metabolism. We then compare the metabolic capabilities of pathogenic and environmental chlamydiae highlighting interspecies variability among the metabolically more flexible environmental strains. We discuss recent findings suggesting that chlamydiae may not live as energy parasites throughout the developmental cycle and that elementary bodies are not metabolically inert but exhibit metabolic activity under appropriate axenic conditions. The observed host-free metabolic activity of elementary bodies may reflect adequate recapitulation of the intracellular environment, but there is evidence that this activity is biologically relevant and required for extracellular survival and maintenance of infectivity. The recent discoveries call for a reconsideration of chlamydial metabolism and future in-depth analyses to better understand how species- and stage-specific differences in chlamydial physiology may affect virulence, tissue tropism, and host adaptation.

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Glucose metabolism by agents of the psittacosis-trachoma group

Cited by 28 publications

References 16 publications

Metabolic Features of Protochlamydia amoebophila Elementary Bodies – A Link between Activity and Infectivity in Chlamydiae

Metabolic Features of Protochlamydia amoebophila Elementary Bodies – A Link between Activity and Infectivity in Chlamydiae

The Relation of the Psittacosis Group (Chlamydiae) to Bacteria and Viruses

Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities

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