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Invasive bronchopulmonary aspergillosis (IBPA) is a life-threatening disease in immunocompromised patients. Although  Aspergillus terreus  is frequently found in the environment,  A. fumigatus  is by far the main cause of IBPA. However, once  A. terreus  establishes infection in the host, disease is as fatal as  A. fumigatus  infections. Thus, we hypothesized that the initial steps of disease establishment might be fundamentally different between these two species. Since alveolar macrophages represent one of the first phagocytes facing inhaled conidia, we compared the interaction of  A. terreus  and  A. fumigatus  conidia with alveolar macrophages.  A. terreus  conidia were phagocytosed more rapidly than  A. fumigatus  conidia, possibly due to higher exposure of β-1,3-glucan and galactomannan on the surface. In agreement, blocking of dectin-1 and mannose receptors significantly reduced phagocytosis of  A. terreus , but had only a moderate effect on phagocytosis of  A. fumigatus . Once phagocytosed, and in contrast to  A. fumigatus ,  A. terreus  did not inhibit acidification of phagolysosomes, but remained viable without signs of germination both  in vitro  and in immunocompetent mice. The inability of  A. terreus  to germinate and pierce macrophages resulted in significantly lower cytotoxicity compared to  A. fumigatus . Blocking phagolysosome acidification by the v-ATPase inhibitor bafilomycin increased  A. terreus  germination rates and cytotoxicity. Recombinant expression of the  A. nidulans wA  naphthopyrone synthase, a homologue of  A. fumigatus  PksP, inhibited phagolysosome acidification and resulted in increased germination, macrophage damage and virulence in corticosteroid-treated mice. In summary, we show that  A. terreus  and  A. fumigatus  have evolved significantly different strategies to survive the attack of host immune cells. While  A. fumigatus  prevents phagocytosis and phagolysosome acidification and escapes from macrophages by germination,  A. terreus  is rapidly phagocytosed, but conidia show long-term persistence in macrophages even in immunocompetent hosts.

Persistence versus Escape: Aspergillus terreus and Aspergillus fumigatus Employ Different Strategies during Interactions with Macrophages