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Virulence Dec 2021The highly contagious whooping cough agent has evolved as a human-restricted pathogen from a progenitor which also gave rise to and . While the latter colonizes a... (Review)
Review
The highly contagious whooping cough agent has evolved as a human-restricted pathogen from a progenitor which also gave rise to and . While the latter colonizes a broad range of mammals and is able to survive in the environment, has lost its ability to survive outside its host through massive genome decay. Instead, it has become a highly successful human pathogen by the acquisition of tightly regulated virulence factors and evolutionary adaptation of its metabolism to its particular niche. By the deployment of an arsenal of highly sophisticated virulence factors it overcomes many of the innate immune defenses. It also interferes with vaccine-induced adaptive immunity by various mechanisms. Here, we review data from , human and animal models to illustrate the mechanisms of adaptation to the human respiratory tract and provide evidence of ongoing evolutionary adaptation as a highly successful human pathogen.
Topics: Animals; Bordetella bronchiseptica; Bordetella parapertussis; Bordetella pertussis; Humans; Mammals; Virulence; Virulence Factors
PubMed: 34590541
DOI: 10.1080/21505594.2021.1980987 -
Pathogens and Disease Nov 2015Bordetella pertussis and B. bronchiseptica are Gram-negative bacterial respiratory pathogens. Bordetella pertussis is the causative agent of whooping cough and is... (Review)
Review
Bordetella pertussis and B. bronchiseptica are Gram-negative bacterial respiratory pathogens. Bordetella pertussis is the causative agent of whooping cough and is considered a human-adapted variant of B. bronchiseptica. Bordetella pertussis and B. bronchiseptica share mechanisms of pathogenesis and are genetically closely related. However, despite the close genetic relatedness, these Bordetella species differ in several classic fundamental aspects of bacterial pathogens such as host range, pathologies and persistence. The development of the baboon model for the study of B. pertussis transmission, along with the development of the swine and mouse model for the study of B. bronchiseptica, has enabled the investigation of different aspects of transmission including the route, attack rate, role of bacterial and host factors, and the impact of vaccination on transmission. This review will focus on B. pertussis transmission and how animal models of B. pertussis transmission and transmission models using the closely related B. bronchiseptica have increased our understanding of B. pertussis transmission.
Topics: Animals; Bordetella bronchiseptica; Bordetella pertussis; Disease Models, Animal; Disease Transmission, Infectious; Humans; Mice; Papio; Swine; Whooping Cough
PubMed: 26374235
DOI: 10.1093/femspd/ftv068 -
Frontiers in Cellular and Infection... 2022A variety of bacteria have evolved the ability to interact with environmental phagocytic predators such as amoebae, which may have facilitated their subsequent...
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 can evade predation by the common soil amoeba , 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 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 species in three assays representing distinct aspects of their interactions with . 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 , and for the human-restricted species and . Interestingly, a different lineage of only known to infect sheep retained the ability to interact with , demonstrating that these abilities were lost in multiple lineages independently, correlating with niche specialization and recent rapid genome decay apparently mediated by insertion sequences. 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 . These results suggest that massive gene loss associated with specialization of some 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.
Topics: Amoeba; Animals; Bordetella; Bordetella bronchiseptica; Dictyostelium; Genome-Wide Association Study; Sheep
PubMed: 35223538
DOI: 10.3389/fcimb.2022.798317 -
Frontiers in Cellular and Infection... 2020Pertussis, also known as whooping cough, is a resurging acute respiratory disease of humans primarily caused by the Gram-negative coccobacilli , and less commonly by the... (Review)
Review
Pertussis, also known as whooping cough, is a resurging acute respiratory disease of humans primarily caused by the Gram-negative coccobacilli , and less commonly by the human-adapted lineage of . The ovine-adapted lineage of infects only sheep, while 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 locus, that encodes components of the type III secretion injectosome, and adjacent 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 is well recognized, the functionality of the type III secretion injectosome in was overlooked for many years due to the adaptation of laboratory-passaged strains. This review highlights the current knowledge of the type III secretion system in the so-called classical species, comprising , and , 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.
Topics: Animals; Bacterial Proteins; Bordetella Infections; Bordetella bronchiseptica; Bordetella pertussis; Sheep; Type III Secretion Systems; Virulence Factors
PubMed: 33014891
DOI: 10.3389/fcimb.2020.00466 -
Trends in Microbiology Feb 2019The mammalian immune system includes a sophisticated array of antimicrobial mechanisms. However, successful pathogens have developed subversive strategies to detect,... (Review)
Review
The mammalian immune system includes a sophisticated array of antimicrobial mechanisms. However, successful pathogens have developed subversive strategies to detect, modulate, and/or evade immune control and clearance. Independent disciplines study host immunology and bacterial pathogenesis, but interkingdom signaling between bacteria and host during natural infection remains poorly understood. An efficient natural host infection system has revealed complex communication between Bordetella spp. and mice, identified novel regulatory mechanisms, and demonstrated that bordetellae can respond to microenvironment and inflammatory status cues. Understanding these bacterial signaling pathways and their complex network that allows precisely timed expression of numerous immunomodulatory factors will serve as a paradigm for other organisms lacking such a powerful experimental infection system. VIDEO ABSTRACT.
Topics: Animals; Bacterial Proteins; Bordetella; Bordetella Infections; Cellular Microenvironment; Environment; Host-Pathogen Interactions; Humans; Immunity, Innate; Immunomodulation; Inflammation; Mice; Signal Transduction; Virulence; Virulence Factors
PubMed: 30661570
DOI: 10.1016/j.tim.2018.09.010 -
Current Opinion in Infectious Diseases Jun 2019To relate genomic changes to phenotypic adaptation and evolution from environmental bacteria to obligate human pathogens, focusing on the examples within Bordetella... (Review)
Review
PURPOSE OF REVIEW
To relate genomic changes to phenotypic adaptation and evolution from environmental bacteria to obligate human pathogens, focusing on the examples within Bordetella species.
RECENT FINDINGS
Recent studies showed that animal-pathogenic and human-pathogenic Bordetella species evolved from environmental ancestors in soil. The animal-pathogenic Bordetella bronchiseptica can hijack the life cycle of the soil-living amoeba Dictyostelium discoideum, surviving inside single-celled trophozoites, translocating to the fruiting bodies and disseminating along with amoeba spores. The association with amoeba may have been a 'training ground' for bacteria during the evolution to pathogens. Adaptation to an animal-associated life style was characterized by decreasing metabolic versatility and genome size and by acquisition of 'virulence factors' mediating the interaction with the new animal hosts. Subsequent emergence of human-specific pathogens, such as Bordetella pertussis from zoonoses of broader host range progenitors, was accompanied by a dramatic reduction in genome size, marked by the loss of hundreds of genes.
SUMMARY
The evolution of Bordetella from environmental microbes to animal-adapted and obligate human pathogens was accompanied by significant genome reduction with large-scale gene loss during divergence.
Topics: Adaptation, Biological; Adaptation, Physiological; Animals; Biological Evolution; Bordetella bronchiseptica; Bordetella pertussis; Host-Pathogen Interactions; Humans; Soil Microbiology
PubMed: 30921085
DOI: 10.1097/QCO.0000000000000549 -
Pathogens and Disease Feb 2016Bordetella bronchiseptica and B. pertussis are Gram-negative bacteria that cause respiratory diseases in animals and humans. The current incidence of whooping cough or... (Review)
Review
Bordetella bronchiseptica and B. pertussis are Gram-negative bacteria that cause respiratory diseases in animals and humans. The current incidence of whooping cough or pertussis caused by B. pertussis has reached levels not observed since the 1950s. Although pertussis is traditionally known as an acute childhood disease, it has recently resurged in vaccinated adolescents and adults. These individuals often become silent carriers, facilitating bacterial circulation and transmission. Similarly, vaccinated and non-vaccinated animals continue to be carriers of B. bronchiseptica and shed bacteria resulting in disease outbreaks. The persistence mechanisms of these bacteria remain poorly characterized. It has been proposed that adoption of a biofilm lifestyle allows persistent colonization of the mammalian respiratory tract. The history of Bordetella biofilm research is only a decade long and there is no single review article that has exclusively focused on this area. We systematically discuss the role of Bordetella factors in biofilm development in vitro and in the mouse respiratory tract. We further outline the implications of biofilms to bacterial persistence and transmission in humans and for the design of new acellular pertussis vaccines.
Topics: Animals; Biofilms; Bordetella Infections; Bordetella bronchiseptica; Bordetella pertussis; Carrier State; Disease Outbreaks; Humans
PubMed: 26586694
DOI: 10.1093/femspd/ftv108 -
Microbiology Spectrum Jun 2023The classical species infect the respiratory tract of mammals. While B. bronchiseptica causes rather chronic respiratory infections in a variety of mammals, the...
The classical species infect the respiratory tract of mammals. While B. bronchiseptica causes rather chronic respiratory infections in a variety of mammals, the human-adapted species B. pertussis and cause an acute respiratory disease known as whooping cough or pertussis. The virulence factors include a type III secretion system (T3SS) that translocates effectors BteA and BopN into host cells. However, the regulatory mechanisms underlying the secretion and translocation activity of T3SS in bordetellae are largely unknown. We have solved the crystal structure of BopN of B. pertussis and show that it is similar to the structures of gatekeepers that control access to the T3SS channel from the bacterial cytoplasm. We further found that BopN accumulates at the cell periphery at physiological concentrations of calcium ions (2 mM) that inhibit the secretion of BteA and BopN. Deletion of the gene in B. bronchiseptica increased secretion of the BteA effector into calcium-rich medium but had no effect on secretion of the T3SS translocon components BopD and BopB. Moreover, the Δ mutant secreted approximately 10-fold higher amounts of BteA into the medium of infected cells than the wild-type bacteria, but it translocated lower amounts of BteA into the host cell cytoplasm. These data demonstrate that BopN is a T3SS gatekeeper required for regulated and targeted translocation of the BteA effector through the T3SS injectisome into host cells. The T3SS is utilized by many Gram-negative bacteria to deliver effector proteins from bacterial cytosol directly into infected host cell cytoplasm in a regulated and targeted manner. Pathogenic bordetellae use the T3SS to inject the BteA and BopN proteins into infected cells and upregulate the production of the anti-inflammatory cytokine interleukin-10 (IL-10) to evade host immunity. Previous studies proposed that BopN acted as an effector in host cells. In this study, we report that BopN is a T3SS gatekeeper that regulates the secretion and translocation activity of T3SS.
Topics: Animals; Humans; Type III Secretion Systems; Whooping Cough; Calcium; Bordetella pertussis; Virulence Factors; Bacterial Proteins; Mammals
PubMed: 37036369
DOI: 10.1128/spectrum.04112-22 -
Frontiers in Immunology 2019Well-adapted pathogens have evolved to survive the many challenges of a robust immune response. Defending against all host antimicrobials simultaneously would be... (Review)
Review
Well-adapted pathogens have evolved to survive the many challenges of a robust immune response. Defending against all host antimicrobials simultaneously would be exceedingly difficult, if not impossible, so many co-evolved organisms utilize immunomodulatory tools to subvert, distract, and/or evade the host immune response. spp. present many examples of the diversity of immunomodulators and an exceptional experimental system in which to study them. Recent advances in this experimental system suggest strategies for interventions that tweak immunity to disrupt bacterial immunomodulation, engaging more effective host immunity to better prevent and treat infections. Here we review advances in the understanding of respiratory pathogens, with special focus on spp., and prospects for the use of immune-stimulatory interventions in the prevention and treatment of infection.
Topics: Bordetella; Bordetella Infections; Humans
PubMed: 31921136
DOI: 10.3389/fimmu.2019.02869 -
Annals of Laboratory Medicine Jul 2021
Review
Topics: Asia; Bordetella; Bordetella Infections; Humans; Pneumonia
PubMed: 33536366
DOI: 10.3343/alm.2021.41.4.439