Genotypic and phenotypic adaptation of pathogens: lesson from the genus Bordetella

Linz, Bodo; Ma, Longhuan; Rivera, Israel; Harvill, Eric T.

doi:10.1097/qco.0000000000000549

Cited by 20 publications

(27 citation statements)

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“…These observations strongly suggest that intracellular survival may be an ancestral trait that might have affected the adaptation of Bordetella spp. from environmental bacteria to mammalian respiratory pathogens (Taylor-Mulneix et al, 2017b;Linz et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…B. petrii was originally isolated from an anaerobic bioreactor culture enriched from river sediment (von Wintzingerode et al, 2001) and was subsequently isolated from many soil samples (Hamidou Soumana et al, 2017;Garrido-Sanz et al, 2018). Although several genomic features have changed throughout their independent evolution, including acquisition and loss of multiple virulence-associated genes (Linz et al, 2016(Linz et al, , 2019, these Bordetella species share many characteristics that make them successful animal pathogens.…”

Section: Introductionmentioning

confidence: 99%

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Conservation of Ancient Genetic Pathways for Intracellular Persistence Among Animal Pathogenic Bordetellae

et al. 2019

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Animal and human pathogens of the genus Bordetella are not commonly considered to be intracellular pathogens, although members of the closely related classical bordetellae are known to enter and persist within macrophages in vitro and have anecdotally been reported to be intracellular in clinical samples. B. bronchiseptica, the species closest to the ancestral lineage of the classical bordetellae, infects a wide range of mammals but is known to have an alternate life cycle, persisting, replicating and disseminating with amoeba. These observations give rise to the hypothesis that the ability for intracellular survival has an ancestral origin and is common among animalpathogenic and environmental Bordetella species. Here we analyzed the survival of B. bronchiseptica and defined its transcriptional response to internalization by murine macrophage-like cell line RAW 264.7. Although the majority of the bacteria were killed and digested by the macrophages, a consistent fraction survived and persisted inside the phagocytes. Internalization prompted the activation of a prominent stress response characterized by upregulation of genes involved in DNA repair, oxidative stress response, pH homeostasis, chaperone functions, and activation of specific metabolic pathways. Cross species genome comparisons revealed that most of these upregulated genes are highly conserved among both the classical and non-classical Bordetella species. The diverse Bordetella species also shared the ability to survive inside RAW 264.7 cells, with the single exception being the bird pathogen B. avium, which has lost several of those genes. Knockout mutations in genes expressed intracellularly resulted in decreased persistence inside the phagocytic cells, emphasizing the importance of these genes in this environment. These data show that the ability to persist inside macrophage-like RAW 264.7 cells is shared among nearly all Bordetella species, suggesting that resisting phagocytes may be an ancient mechanism that precedes speciation in the genus and may have facilitated the adaptation of Bordetella species from environmental bacteria to mammalian respiratory pathogens.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Conservation of Ancient Genetic Pathways for Intracellular Persistence Among Animal Pathogenic Bordetellae

et al. 2019

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“…But although B. pertussis has lost over 20% of its genome since diverging from B. bronchiseptica, the Bvg regulon in B. pertussis is largely conserved, demonstrating that the system has been under purifying selection. In addition, the ability to switch between life styles seems to be conserved among the bordetellae, as bvgA and bvgS gene homologs have been found in the genomes of animal-associated species as well as of the environmental B. petrii (Gerlach et al, 2004;Gross et al, 2010;Linz et al, 2016Linz et al, , 2019, contradicting the "vestigial" hypothesis.…”

Section: The Virulence-repressed Bvg − Phase and The Environmentmentioning

confidence: 98%

“…The biological significance of the Bvg − phase has long been hypothetical, mainly due to the lack of a clear role for the virulence-repressed state during in vivo studies and lack of knowledge of ex vivo growth. Several authors have speculated that activation of virulence-repressed genes might serve a role during persistence in an environmental reservoir (Cotter and Miller, 1994;Hamidou Soumana et al, 2017;Moon et al, 2017;Taylor-Mulneix et al, 2017b;Linz et al, 2019). Since many of the Bvg − phase transcribed genes are predicted to be metabolic enzymes and transport proteins, they are suspected to enhance acquisition of nutrients, growth, and proliferation in environmental settings.…”

Section: The Virulence-repressed Bvg − Phase and The Environmentmentioning

confidence: 99%

Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells

2020

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The classical bordetellae possess several partially characterized virulence mechanisms that are studied in the context of a complete extracellular life cycle in their mammalian hosts. Yet, classical bordetellae have repeatedly been reported within dendritic cells (DCs) and alveolar macrophages in clinical samples, and in vitro experiments convincingly demonstrate that the bacteria can survive intracellularly within mammalian phagocytic cells, an ability that appears to have descended from ancestral progenitor species that lived in the environment and acquired the mechanisms to resist unicellular phagocytic predators. Many pathogens, including Mycobacterium tuberculosis, Salmonella enterica, Francisella tularensis, and Legionella pneumophila, are known to parasitize and multiply inside eukaryotic host cells. This strategy provides protection, nutrients, and the ability to disseminate systemically. While some work has been dedicated at characterizing intracellular survival of Bordetella pertussis, there is limited understanding of how this strategy has evolved within the genus Bordetella and the contributions of this ability to bacterial pathogenicity, evasion of host immunity as well as within and between-host dissemination. Here, we explore the mechanisms that control the metabolic changes accompanying intracellular survival and how these have been acquired and conserved throughout the evolutionary history of the Bordetella genus and discuss the possible implications of this strategy in the persistence and reemergence of B. pertussis in recent years.

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“…The phylogenetic analysis of the genus suggests that the animal-associated species likely evolved from their ancestors living in soil and/or water (Hamidou Soumana et al, 2017 ). The diversification and speciation in the genus were accompanied by the gain and loss of multiple genes, including genes for bacterial protein toxins, protein secretion systems, and other virulence factors (Linz et al, 2016 , 2019 ). The presence of the genes encoding Bordetella protein toxins, consisting of adenylate cyclase toxin, pertussis toxin, and dermonecrotic toxin distinguishes classical Bordetella species from the non-classical bordetellae (Linz et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Bordetella Type III Secretion Injectosome and Effector Proteins

Kamanová

2020

Front. Cell. Infect. Microbiol.

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Pertussis, also known as whooping cough, is a resurging acute respiratory disease of humans primarily caused by the Gram-negative coccobacilli Bordetella pertussis, and less commonly by the human-adapted lineage of B. parapertussis HU. The ovine-adapted lineage of B. parapertussis OV infects only sheep, while B. bronchiseptica causes chronic and often asymptomatic respiratory infections in a broad range of mammals but rarely in humans. A largely overlapping set of virulence factors inflicts the pathogenicity of these bordetellae. Their genomes also harbor a pathogenicity island, named bsc locus, that encodes components of the type III secretion injectosome, and adjacent btr locus with the type III regulatory proteins. The Bsc injectosome of bordetellae translocates the cytotoxic BteA effector protein, also referred to as BopC, into the cells of the mammalian hosts. While the role of type III secretion activity in the persistent colonization of the lower respiratory tract by B. bronchiseptica is well recognized, the functionality of the type III secretion injectosome in B. pertussis was overlooked for many years due to the adaptation of laboratory-passaged B. pertussis strains. This review highlights the current knowledge of the type III secretion system in the so-called classical Bordetella species, comprising B. pertussis, B. parapertussis, and B. bronchiseptica, and discusses its functional divergence. Comparison with other well-studied bacterial injectosomes, regulation of the type III secretion on the transcriptional and post-transcriptional level, and activities of BteA effector protein and BopN protein, homologous to the type III secretion gatekeepers, are addressed.

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Genotypic and phenotypic adaptation of pathogens: lesson from the genus Bordetella

Cited by 20 publications

References 49 publications

Conservation of Ancient Genetic Pathways for Intracellular Persistence Among Animal Pathogenic Bordetellae

Conservation of Ancient Genetic Pathways for Intracellular Persistence Among Animal Pathogenic Bordetellae

Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells

Bordetella Type III Secretion Injectosome and Effector Proteins

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