Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells

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 cl...

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Main Authors: Israel Rivera, Bodo Linz, Eric T. Harvill
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.557819/full
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author Israel Rivera
Bodo Linz
Bodo Linz
Eric T. Harvill
author_facet Israel Rivera
Bodo Linz
Bodo Linz
Eric T. Harvill
author_sort Israel Rivera
collection DOAJ
description 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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spelling doaj.art-dae1597aaf7d48a190228911c053eb112022-12-21T23:57:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-10-011110.3389/fmicb.2020.557819557819Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host CellsIsrael Rivera0Bodo Linz1Bodo Linz2Eric T. Harvill3Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA, United StatesDepartment of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA, United StatesDivision of Microbiology, Department of Biology, Friedrich Alexander University Erlangen-Nuremberg, Erlangen, GermanyDepartment of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA, United StatesThe 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.https://www.frontiersin.org/article/10.3389/fmicb.2020.557819/fullBordetellaevolutionintracellular survivalphagocytestranscriptome
spellingShingle Israel Rivera
Bodo Linz
Bodo Linz
Eric T. Harvill
Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells
Frontiers in Microbiology
Bordetella
evolution
intracellular survival
phagocytes
transcriptome
title Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells
title_full Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells
title_fullStr Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells
title_full_unstemmed Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells
title_short Evolution and Conservation of Bordetella Intracellular Survival in Eukaryotic Host Cells
title_sort evolution and conservation of bordetella intracellular survival in eukaryotic host cells
topic Bordetella
evolution
intracellular survival
phagocytes
transcriptome
url https://www.frontiersin.org/article/10.3389/fmicb.2020.557819/full
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