Invasion of Protozoa by Legionella pneumophila and Its Role in Bacterial Ecology and Pathogenesis

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The first recognized outbreak of pneumonia due to Legionella pneumophila occurred in Philadelphia, Pa., in July of 1976 among 180 persons attending the 56th annual American Legion Convention. Twenty-nine patients died, and the disease became known as Legionnaires’ disease (23). Guinea pigs were infected with postmortem lung tissue from the patients with fatal Legionnaires’ disease, and embryonated yolk sacs were inoculated with spleen homogenates from the infected guinea pigs. In January of 1977, a gram-negative bacterium was isolated and designated L. pneumophila (36). The source of the infection during the Legionnaires’ convention was later found to be the air-conditioning system in the hotel. It has been documented that the hallmark of Legionnaires’ disease is the intracellular replication of L. pneumophila in alveolar spaces. At least 39 species of legionellae have been identified. Some of these are associated with disease, while others are environmental isolates; whether the latter can cause disease is not known. L. pneumophila is responsible for more than 80% of cases of Legionnaires’ disease, and among the 13 serogroups of L. pneumophila, serogroup 1 is responsible for more than 95% of Legionnaires’ disease cases. It is estimated that L. pneumophila is responsible for at least 25,000 cases of pneumonia per year in the United States, which is very probably an underestimate due to the difficulty of isolating bacteria from clinical samples. Since L. pneumophila is the most frequent cause of Legionnaires’ disease, most pathogenic and environmental studies have focused on L. pneumophila. In 1980, Rowbotham described the ability of L. pneumophila to multiply intracellularly within protozoa (40). Since then, L. pneumophila has been described to multiply in many species of protozoa, and this host-parasite interaction is central to the pathogenesis and ecology of L. pneumophila. Intracellular replication of L. pneumophila within mammalian and protozoan cells has been shown to occur in a ribosome-studded phagosome that does not fuse to lysosomes. Fields hypothesized that the L. pneumophila phagosome fuses to the rough endoplasmic reticulum (RER) (20). Immunocytochemistry has proven this prediction by demonstrating the presence of an RER-specific chaperon, the Bip protein, in ribosome-studded phagosomes within macrophages (45) and protozoa (1). Based on these characteristics, the L. pneumophila phagosome may be accurately described as an endosomal maturation-blocked (EMB) phagosome.