Potential role of bacteria packaging by protozoa in the persistence and transmission of pathogenic bacteria

Abstract

Many pathogenic bacteria live in close association with protozoa. These unicellular eukaryotic microorganisms are ubiquitous in various environments. A number of protozoa such as amoebae and ciliates ingest pathogenic bacteria, package them usually in membrane structures, and then release them into the environment. Packaged bacteria are more resistant to various stresses and are more apt to survive than free bacteria. New evidence indicates that protozoa and not bacteria control the packaging process. It is possible that packaging is more common than suspected and may play a major role in the persistence and transmission of pathogenic bacteria. To confirm the role of packaging in the propagation of infections, it is vital that the molecular mechanisms governing the packaging of bacteria by protozoa be identified as well as elements related to the ecology of this process in order to determine whether packaging acts as a Trojan Horse.

Keywords: Legionella pneumophila; amoeba; bacteria packaging; multilamellar body; mycobacteria; persistence; protozoa; transmission.

Figure 1

Bacteria packaging by amoebae. (A) Schematic diagram of the packaging process that allows packaged bacteria to resist lysosomal degradation (Res. B), unlike digestible bacteria (Dig. B). The resisting bacteria are packaged in multilamellar bodies (MLB) and are then secreted by the amoebae. (B) Transmission electron microscopic image of L. pneumophila bacteria (black ovoid forms) packaged in a MLB produced and secreted by A. castellanii. Image reproduced from Berk et al. (1998) with the permission of the American Society for Microbiology. (C) Transmission electron microscopic image of a MLB devoid of bacteria produced and secreted by D. discoideum DH1-10 (Cornillon et al., 2000) grown on digestible bacteria, which were a laboratory strain of K. aerogenes (Benghezal et al., 2006). Scale bar = 1 μm in (B,C).

Figure 2

MLBs secreted by D. discoideum cells grown on Gram-positive bacteria. Transmission electron microscopic images of MLBs secreted by D. discoideum DH1-10 cells (Cornillon et al., 2000) grown on B. subtilis (Benghezal et al., 2006) (A,B) and M. luteus ATCC 4698 (C). One MLB is shown in each panel. Scale bars = 0.2 μm.

Figure 3

D. discoideum cells can package polystyrene beads in secreted MLBs. Transmission electronic micrographic images of polystyrene beads packaged in thick (A) and thin (B) MLBs after being incubated with D. discoideum DH1-10 cells (Cornillon et al., 2000) in the presence of digestible bacteria. Scale bars = 0.2 μm.

Figure 4

Intra-lysosomal profile of D. discoideum cells fed digestible bacteria. (A) Transmission electronic micrographic image of a D. discoideum DH1-10 cell (Cornillon et al., 2000) with a lysosomal compartment displaying an intra-lysosomal profile (white square) and a MLB inside a lysosomal compartment (white arrow). B. Magnification of image A showing the inward bud in greater detail. The inward budding is in a lysosomal compartment containing no other electron dense material. The invaginations of the lysosomal membrane are hard to detect in compartments already containing MLBs because the compartments are too crowded. Scale bar = 2 μm in (A) and 0.2 μm in (B).