The Intracellular Bacteria Chlamydia Hijack Peroxisomes and Utilize Their Enzymatic Capacity to Produce Bacteria-Specific Phospholipids

Gaelle Boncompain,Agathe Subtil,Constanze Müller,Paul B Lazarow,Vannary Meas-Yedid,Philippe Schmitt-Kopplin,Thomas Rudel

doi:10.1371/journal.pone.0086196

Abstract

Chlamydia trachomatis is an obligate intracellular pathogen responsible for loss of eyesight through trachoma and for millions of cases annually of sexually transmitted diseases. The bacteria develop within a membrane-bounded inclusion. They lack enzymes for several biosynthetic pathways, including those to make some phospholipids, and exploit their host to compensate. Three-dimensional fluorescence microscopy demonstrates that small organelles of the host, peroxisomes, are translocated into the Chlamydia inclusion and are found adjacent to the bacteria. In cells deficient for peroxisome biogenesis the bacteria are able to multiply and give rise to infectious progeny, demonstrating that peroxisomes are not essential for bacterial development in vitro. Mass spectrometry-based lipidomics reveal the presence in C. trachomatis of plasmalogens, ether phospholipids whose synthesis begins in peroxisomes and have never been described in aerobic bacteria before. Some of the bacterial plasmalogens are novel structures containing bacteria-specific odd-chain fatty acids; they are not made in uninfected cells nor in peroxisome-deficient cells. Their biosynthesis is thus accomplished by the metabolic collaboration of peroxisomes and bacteria.

Highlights

Chlamydia are Gram-negative bacteria, which infect a wide range of hosts
Host glycerophospholipids are not merely incorporated by the bacteria but some serve as precursors for bacteria-specific lipids: the sn-2 position fatty acid of the host phospholipids is removed and replaced with a Chlamydia-synthesized branched chain fatty acid with an odd number of carbons [6]
Since lipid droplets (LD) are imported into inclusions and peroxisomes are often associated with LD, we investigated whether peroxisomes might be imported into inclusions and exploited by the bacteria

Summary

Introduction

Chlamydia are Gram-negative bacteria, which infect a wide range of hosts. They are obligate intracellular pathogens and multiply within mucosal epithelial cells. Some bacterial phospholipids differ from those of the host cells, which have straight-chain fatty acids with an even number of carbons. Peroxisomes were observed inside the inclusion, often adjacent to anti-Hsp60 labeled bacteria (Figure 1B).

Results

Conclusion