Microorganisms resistant to free-living amoebae

Abstract

Free-living amoebae feed on bacteria, fungi, and algae. However, some microorganisms have evolved to become resistant to these protists. These amoeba-resistant microorganisms include established pathogens, such as Cryptococcus neoformans, Legionella spp., Chlamydophila pneumoniae, Mycobacterium avium, Listeria monocytogenes, Pseudomonas aeruginosa, and Francisella tularensis, and emerging pathogens, such as Bosea spp., Simkania negevensis, Parachlamydia acanthamoebae, and Legionella-like amoebal pathogens. Some of these amoeba-resistant bacteria (ARB) are lytic for their amoebal host, while others are considered endosymbionts, since a stable host-parasite ratio is maintained. Free-living amoebae represent an important reservoir of ARB and may, while encysted, protect the internalized bacteria from chlorine and other biocides. Free-living amoebae may act as a Trojan horse, bringing hidden ARB within the human "Troy," and may produce vesicles filled with ARB, increasing their transmission potential. Free-living amoebae may also play a role in the selection of virulence traits and in adaptation to survival in macrophages. Thus, intra-amoebal growth was found to enhance virulence, and similar mechanisms seem to be implicated in the survival of ARB in response to both amoebae and macrophages. Moreover, free-living amoebae represent a useful tool for the culture of some intracellular bacteria and new bacterial species that might be potential emerging pathogens.

FIG. 1.

The two developmental stages of Hartmanella vermiformis. (A) The trophozoite, a vegetative feeding form; (B) the cyst, a resting form. Bar, 2 μm. Magnifications, ×5,325 (A) and ×6,675 (B).

FIG.2.

The role of free-living amoebae as a reservoir of intracellular bacteria, as a Trojan horse, in the transmission of its bacterial host, in the selection of virulence traits, and in the adaptation of the bacteria to macrophages. The bacteria are shown in red, the amoebae are shown in grey, and their mitochondria are shown in green. (Top) Life cycle of amoeba-resistant bacteria within amoebae present in the environment or in the nasal mucosa. (Bottom) Amoeba-resistant microorganisms in the lower respiratory tract. During the cycle of intra-amoebal replication, bacteria select virulence traits. Moreover, amoebal vacuoles represent an important reservoir of bacteria, which may reach alveolar macrophages within amoebae, within expelled vesicles, or free. The strategy of resistance to macrophage microbicidal effectors varies from species to species and might have been acquired following exposure to environmental predators such as free-living amoebae.

FIG. 3.

Gimenez-stained ARB. B. vestrisii is shown within A. polyphaga in a laboratory infection. Gimenez staining. Magnification, ×750.

FIG. 4.

L. pneumophila within H. vermiformis in a laboratory infection. Magnification, ×16,500. Bar, 0.5 μm.

FIG. 5.

A. polyphaga filled with P. acanthamoebae in a laboratory infection. Crescent bodies may be seen (arrow). Magnification, ×2,625. Bar, 1 μm.

FIG. 6.

Mimivirus, a giant virus naturally infecting free-living amoebae. (A) Mimivirus and A. polyphaga, as seen by scanning electron microscopy. Bar, 1 μm. (B) Mimivirus. Negative coloration, as seen by transmission electron microscopy. Bar, 200 nm. (C) Mimivirus within A. polyphaga in a laboratory infection, as seen by transmission electron microscopy. Bar, 2 μm. Magnifications, ×3,375 (A), ×33,750 (B), and 3,000 (C). Reprinted with permission from B. La Scola (A and C) and N. Aldrovandi (B).

FIG.7.

Phagocytosis of L. pneumophila by H. vermiformis in a laboratory infection. (A) Adherence; (B) uptake; (C) internalized bacteria. mi, mitochondria. Magnification, ×22,000. Bar, 0.5 μm.