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Although filamentous morphology in bacteria has been associated with resistance to phagocytosis, our understanding of the cellular mechanisms behind this process is limited. To investigate this, we followed the phagocytosis of both viable and dead Legionella pneumophila filaments. The engulfment of these targets occurred gradually and along the longitudinal axis of the filament, therefore defining a long-lasting phagocytic cup stage that determined the outcome of phagocytosis. We found that these phagocytic cups fused with endosomes and lysosomes, events linked to the maturation of phagosomes according to the canonical pathway, and not with the remodeling of phagocytic cups. Nevertheless, despite acquiring phagolysosomal features these phagocytic cups failed to develop hydrolytic capacity before their sealing. This phenomenon hampered the microbicidal activity of the macrophage and enhanced the capacity of viable filamentous L. pneumophila to escape phagosomal killing in a length-dependent manner. Our results demonstrate that key aspects in phagocytic cup remodeling and phagosomal maturation could be influenced by target morphology.

Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages