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Abstract
A variety of bacteria have evolved the ability to interact with environmental phagocytic predators such as amoebae, which may have facilitated their subsequent interactions with phagocytes in animal hosts. Our recent study found that the animal pathogen Bordetella bronchiseptica can evade predation by the common soil amoeba Dictyostelium discoideum, survive within, and hijack its complex life cycle as a propagation and dissemination vector. However, it is uncertain whether the mechanisms allowing interactions with predatory amoebae are conserved among Bordetella species, because divergence, evolution, and adaptation to different hosts and ecological niches was accompanied by acquisition and loss of many genes. Here we tested 9 diverse Bordetella species in three assays representing distinct aspects of their interactions with D. discoideum. Several human and animal pathogens retained the abilities to survive within single-celled amoeba, to inhibit amoebic plaque expansion, and to translocate with amoebae to the fruiting body and disseminate along with the fruiting body. In contrast, these abilities were partly degraded for the bird pathogen B. avium, and for the human-restricted species B. pertussis and B. parapertussis. Interestingly, a different lineage of B. parapertussis only known to infect sheep retained the ability to interact with D. discoideum, demonstrating that these abilities were lost in multiple lineages independently, correlating with niche specialization and recent rapid genome decay apparently mediated by insertion sequences. B. petrii has been isolated sporadically from diverse human and environmental sources, has acquired insertion sequences, undergone genome decay and has also lost the ability to interact with amoebae, suggesting some specialization to some unknown niche. A genome-wide association study (GWAS) identified a set of genes that are potentially associated with the ability to interact with D. discoideum. These results suggest that massive gene loss associated with specialization of some Bordetella species to a closed life cycle in a particular host was repeatedly and independently accompanied by loss of the ability to interact with amoebae in an environmental niche.
Highlights
The genus Bordetella comprises 16 named species, including the “classical” species consisting of B. bronchiseptica, B. pertussis and B. parapertussis
To compare the intracellular survival of classical Bordetella species inside D. discoideum, a gentamicin protection assay was performed after exposure of B. bronchiseptica, B. pertussis, B. parapertussishu, B. parapertussisov or K. pneumoniae, a food resource bacterium of amoeba, to a confluent monolayer of D. discoideum for 45 minutes
In contrast to K. pneumoniae, which was undetectable in this assay, more than two thousand viable B. bronchiseptica and B. parapertussisov cells were consistently recovered from the unicellular amoeba, which represented over two percent of the inoculated bacteria
Summary
The genus Bordetella comprises 16 named species, including the “classical” species consisting of B. bronchiseptica, B. pertussis and B. parapertussis. The classical Bordetella species are found in mammalian hosts, as B. pertussis infects humans, the two lineages of B. parapertussis infect either humans (B. parapertussishu) or sheep (B. parapertussisov), and B. bronchiseptica is a pathogen of a wide range of mammals (Mattoo and Cherry, 2005). More distantly related species, often referred to as the non-classical Bordetella species, cause infections in a variety of hosts, including B. holmesii in humans (Weyant et al, 1995), B. avium and B. hinzii in birds (Raffel et al, 2002; Register and Kunkle, 2009), and B. pseudohinzii in rodents (Ivanov et al, 2015; Ivanov et al, 2016). B. petrii has been isolated from multiple natural environments, including an anaerobic, dechlorinating bioreactor culture enriched by river sediment, marine sponges and grass root consortia (von Wintzingerode et al, 2001)
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