Abstract

The order Chlamydiales includes obligate intracellular pathogens capable of infecting mammals, fishes and amoeba. Unlike other intracellular bacteria for which intracellular adaptation led to the loss of glycogen metabolism pathway, all chlamydial families maintained the nucleotide-sugar dependent glycogen metabolism pathway i.e. the GlgC-pathway with the notable exception of both Criblamydiaceae and Waddliaceae families. Through detailed genome analysis and biochemical investigations, we have shown that genome rearrangement events have resulted in a defective GlgC-pathway and more importantly we have evidenced a distinct trehalose-dependent GlgE-pathway in both Criblamydiaceae and Waddliaceae families. Altogether, this study strongly indicates that the glycogen metabolism is retained in all Chlamydiales without exception, highlighting the pivotal function of storage polysaccharides, which has been underestimated to date. We propose that glycogen degradation is a mandatory process for fueling essential metabolic pathways that ensure the survival and virulence of extracellular forms i.e. elementary bodies of Chlamydiales.

Highlights

  • The order Chlamydiales includes obligate intracellular pathogens capable of infecting mammals, fishes and amoeba

  • The formation of α-1,6 linkages and glycogen degradation are catalyzed by a set of similar enzymes in both pathways that include glycogen branching enzyme isoforms (GlgB/GlgB2) and glycogen phosphorylases isoforms (GlgP/GlgP2), glycogen debranching enzymes (GlgX) and glycogen phosphorylases isoforms The genomic database used in this study includes genomes from both cultured and uncultured Chlamydiae species that cover the diversity of the chlamydiae phylum (Fig. 1b)

  • This gene is missing from six independent draft genomes estimated to be 71–97% complete, suggesting either the loss of glgC gene or that glgC gene is located in a particular genomic region that systematically led to its absence from genome assemblies

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Summary

Introduction

The order Chlamydiales includes obligate intracellular pathogens capable of infecting mammals, fishes and amoeba. All Chlamydiales display an obligate intracellular lifestyle due to a massive genome reduction and biphasic development, which includes two major morphological and physiological distinct stages: the elementary body (EB), a non-dividing and infectious form adapted to extracellular survival and the reticulate body (RB), a replicating form located within a membrane surrounded inclusion Despite the more advanced genome reduction experienced by the animalspecific Chlamydiaceae family (0.9 Mpb) in comparison to other protist-infecting Chlamydiales (2–2.5 Mpb), the glycogen metabolism pathway appears surprisingly preserved[7]. This includes the three-enzymatic activities required for glycogen biosynthesis: GlgC, GlgA, and GlgB9. When the primer reaches a sufficient degree of polymerization (DP > 15) to fit the catalytic site of the glycogen branching enzyme (GlgB), glycogen branching introduced resulting in the appearance of two nonreducing polymer ends that may be further elongated by GlgA

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