-
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 -
Toxins Jan 2021The adenylate cyclase toxin, CyaA, is one of the key virulent factors produced by , the causative agent of whooping cough. This toxin primarily targets innate immunity... (Review)
Review
The adenylate cyclase toxin, CyaA, is one of the key virulent factors produced by , the causative agent of whooping cough. This toxin primarily targets innate immunity to facilitate bacterial colonization of the respiratory tract. CyaA exhibits several remarkable characteristics that have been exploited for various applications in vaccinology and other biotechnological purposes. CyaA has been engineered as a potent vaccine vehicle to deliver antigens into antigen-presenting cells, while the adenylate cyclase catalytic domain has been used to design a robust genetic assay for monitoring protein-protein interactions in bacteria. These two biotechnological applications are briefly summarized in this chapter.
Topics: Adenylate Cyclase Toxin; Animals; Bioengineering; Bordetella pertussis; Humans; Pertussis Vaccine; Protein Engineering; Two-Hybrid System Techniques; Whooping Cough
PubMed: 33499260
DOI: 10.3390/toxins13020083 -
Postepy Higieny I Medycyny... May 2017Bordetella pertussis strains, which have lost the ability to produce antigens, such as pertactin - Prn, pertussis toxin - Ptx, filamentous haemagglutinin - FHA, fimbriae... (Review)
Review
Bordetella pertussis strains, which have lost the ability to produce antigens, such as pertactin - Prn, pertussis toxin - Ptx, filamentous haemagglutinin - FHA, fimbriae type 2 and 3 - Fim 2 and 3, tracheal colonization factor - TcfA, have recently been isolated in countries with a high vaccination coverage. The emergence of such isolates might have resulted from B. pertussis natural evolution course or adaptive mechanisms, allowing increased circulation of the pathogen in vaccinated populations. So far, the majority of described mutants were deficient in the Prn production. Prn deficient isolates were found in countries which use acellular pertussis vaccines (aP) in routine immunization programmes. The increase of frequency of Prn¯ strains isolation was correlated with the period of routine vaccination with aP vaccines. In most countries, the spread of these isolates has resulted from independent mutations rather than from the expansion of a single clone. Prn¯ isolates were collected from patients showing typical clinical symptoms of pertussis found for Prn+ strains. Results of in vitro and in vivo studies have shown that Prn¯, Ptx¯ and FHA¯ isolates retain cytotoxic properties, and besides Ptx¯ isolates, were lethal in intranasally infected mice. Further explanation of the impact of antigen deficiencies on virulence and transmission of B. pertussis in the context of the continuous increase of pertussis incidence is necessary to develop a new, optimized strategy of pertussis prevention.
Topics: Animals; Bordetella pertussis; Humans; Mice; Pertussis Vaccine; Virulence Factors, Bordetella; Whooping Cough
PubMed: 28513461
DOI: 10.5604/01.3001.0010.3821 -
Infection and Immunity Nov 2021Bordetella pertussis is a highly contagious bacterium that is the causative agent of whooping cough (pertussis). Currently, acellular pertussis vaccines (aP, DTaP, and...
Bordetella pertussis is a highly contagious bacterium that is the causative agent of whooping cough (pertussis). Currently, acellular pertussis vaccines (aP, DTaP, and Tdap) are used to prevent pertussis disease. However, it is clear that the aP vaccine efficacy quickly wanes, resulting in the reemergence of pertussis. Furthermore, recent work performed by the CDC suggest that current circulating strains are genetically distinct from strains of the past. The emergence of genetically diverging strains, combined with waning aP vaccine efficacy, calls for reevaluation of current animal models of pertussis. In this study, we used the rat model of pertussis to compare two genetically divergent strains Tohama 1 and D420. We intranasally challenged 7-week-old Sprague-Dawley rats with 10 viable Tohama 1 and D420 and measured the hallmark signs/symptoms of infection such as neutrophilia, pulmonary inflammation, and paroxysmal cough using whole-body plethysmography. Onset of cough occurred between 2 and 4 days after challenge, averaging five coughs per 15 min, with peak coughing occurring at day 8 postinfection, averaging upward of 13 coughs per 15 min. However, we observed an increase of coughs in rats infected with clinical isolate D420 through 12 days postchallenge. The rats exhibited increased bronchial restriction following infection. Histology of the lung and flow cytometry confirm both cellular infiltration and pulmonary inflammation. D420 infection induced higher production of anti- IgM antibodies compared to Tohama 1 infection. The coughing rat model provides a way of characterizing disease manifestation differences between strains.
Topics: Animals; Biomarkers; Bordetella pertussis; Disease Models, Animal; Disease Susceptibility; Host-Pathogen Interactions; Rats; Whooping Cough
PubMed: 34125597
DOI: 10.1128/IAI.00304-21 -
Emerging Infectious Diseases Jun 2019During the 2008-2012 pertussis epidemic in Australia, pertactin (Prn)-negative Bordetella pertussis emerged. We analyzed 78 isolates from the 2013-2017 epidemic and...
During the 2008-2012 pertussis epidemic in Australia, pertactin (Prn)-negative Bordetella pertussis emerged. We analyzed 78 isolates from the 2013-2017 epidemic and documented continued expansion of Prn-negative ptxP3 B. pertussis strains. We also detected a filamentous hemagglutinin-negative and Prn-negative B. pertussis isolate.
Topics: Adhesins, Bacterial; Alleles; Australia; Bacterial Outer Membrane Proteins; Bordetella pertussis; History, 21st Century; Humans; Pertussis Vaccine; Phylogeny; Virulence Factors, Bordetella; Whooping Cough
PubMed: 31107218
DOI: 10.3201/eid2506.180240 -
FEMS Microbiology Reviews May 2011Pertussis, or whooping cough, is a highly contagious, acute respiratory disease of humans that is caused by the Gram-negative bacterial pathogen Bordetella pertussis. In... (Review)
Review
Pertussis, or whooping cough, is a highly contagious, acute respiratory disease of humans that is caused by the Gram-negative bacterial pathogen Bordetella pertussis. In the face of extensive global vaccination, this extremely monomorphic pathogen has persisted and re-emerged, causing approximately 300,000 deaths each year. In this review, we discuss the interaction of B. pertussis with the host mucosal epithelium and immune system. Using a large number of virulence factors, B. pertussis is able to create a niche for colonization in the human respiratory tract. The successful persistence of this pathogen is mainly due to its ability to interfere with almost every aspect of the immune system, from the inhibition of complement- and phagocyte-mediated killing to the suppression of T- and B-cell responses. Based on these insights, we delineate ideas for the rational design of improved vaccines that can target the 'weak spots' in the pathogenesis of this highly successful pathogen.
Topics: Animals; Bordetella pertussis; Humans; Mice; Virulence Factors; Whooping Cough
PubMed: 21204863
DOI: 10.1111/j.1574-6976.2010.00257.x -
Emerging Microbes & Infections Dec 2021Respiratory infections caused by are reemerging despite high pertussis vaccination coverage. Since the introduction of the acellular pertussis vaccine in the late...
Respiratory infections caused by are reemerging despite high pertussis vaccination coverage. Since the introduction of the acellular pertussis vaccine in the late twentieth century, circulating strains increasingly lack expression of the vaccine component pertactin (Prn). In some countries, up to 90% of the circulating strains are deficient in Prn. To better understand the resurgence of pertussis, we investigated the response of human monocyte-derived dendritic cells (moDCs) to naturally circulating Prn-expressing (Prn-Pos) and Prn-deficient (Prn-Neg) strains from 2016 in the Netherlands. Transcriptome analysis of moDC showed enriched IFNα response-associated gene expression after exposure to Prn-Pos strains, whereas the Prn-Neg strains induced enriched expression of interleukin- and TNF-signaling genes, as well as other genes involved in immune activation. Multiplex immune assays confirmed enhanced proinflammatory cytokine secretion by Prn-Neg stimulated moDC. Comparison of the proteomes from the Prn-Pos and Prn-Neg strains revealed, next to the difference in Prn, differential expression of a number of other proteins including several proteins involved in metabolic processes. Our findings indicate that Prn-deficient strains induce a distinct and stronger immune activation of moDCs than the Prn-Pos strains. These findings highlight the role of pathogen adaptation in the resurgence of pertussis as well as the effects that vaccine pressure can have on a bacterial population.
Topics: Adaptation, Biological; Bacterial Outer Membrane Proteins; Bordetella pertussis; Cytokines; Dendritic Cells; Gene Expression Profiling; Host-Pathogen Interactions; Humans; Inflammation; Pertussis Vaccine; Toll-Like Receptor 2; Toll-Like Receptor 4; Transcriptome; Virulence Factors, Bordetella; Whooping Cough
PubMed: 34132167
DOI: 10.1080/22221751.2021.1943537 -
Archivum Immunologiae Et Therapiae... Dec 2013Approximately 40 million whooping cough cases and between 200,000 and 400,000 pertussis-linked deaths are recorded each year. Although several types of vaccines are... (Review)
Review
Approximately 40 million whooping cough cases and between 200,000 and 400,000 pertussis-linked deaths are recorded each year. Although several types of vaccines are licensed and widely used, Bordetella pertussis continues to circulate in populations with high vaccine coverage of infants and children due to the waning of protection induced by the vaccination. B. pertussis typically expresses a wide array of virulence factors which promote bacterial adhesion and invasion by altering the local environment, including pertussis toxin, tracheal cytotoxin, adenylate cyclase toxin, filamentous hemagglutinin, and the lipooligosaccharide. The virulence factors of B. pertussis also possess immunomodulatory properties, exerted through their enzymatic and receptor-binding activities. Both pro- and anti-inflammatory effects are mediated, that can subvert host innate and adaptive immunity and favor the onset of a long-term infection. This review describes the capacities of B. pertussis virulence factors to modulate host immune responses and the mechanisms employed, which have been the subject of extensive research in the recent years, both in murine and human experimental systems. Knowledge of these mechanisms is gaining increasing importance, since it could provide in the near future the basis for the identification of therapeutic agents for modulating the immune system as well as novel molecular targets to treat pertussis.
Topics: Animals; Bacterial Toxins; Bordetella pertussis; Cellular Microenvironment; Child; Disease Models, Animal; Host-Pathogen Interactions; Humans; Immune Evasion; Immunity, Innate; Immunomodulation; Infant; Mice; Virulence Factors; Whooping Cough
PubMed: 23955529
DOI: 10.1007/s00005-013-0242-1 -
Microbial Genomics May 2018Bordetella pertussis, the causative agent of whooping cough, has experienced a resurgence in the past 15 years, despite the existence of both whole-cell and acellular...
Bordetella pertussis, the causative agent of whooping cough, has experienced a resurgence in the past 15 years, despite the existence of both whole-cell and acellular vaccines. Here, we performed whole genome sequencing analysis of 149 clinical strains, provided by the National Institute of Infectious Diseases (NIID), Japan, isolated in 1982-2014, after Japan became the first country to adopt acellular vaccines against B. pertussis. Additionally, we sequenced 39 strains provided by the Konan Kosei Hospital in Aichi prefecture, Japan, isolated in 2008-2013. The genome sequences afforded insight into B. pertussis genome variability and population dynamics in Japan, and revealed that the B. pertussis population in Japan was characterized by two major clades that divided more than 40 years ago. The pertactin gene was disrupted in about 20 % of the 149 NIID isolates, by either a deletion within the signal sequence (ΔSS) or the insertion of IS element IS481 (prn :: IS481). Phylogeny suggests that the parent clones for these isolates originated in Japan. Divergence dating traced the first generation of the pertactin-deficient mutants in Japan to around 1990, and indicated that strains containing the alternative pertactin allele prn2 may have appeared in Japan around 1974. Molecular clock data suggested that observed fluctuations in B. pertussis population size may have coincided with changes in vaccine usage in the country. The continuing failure to eradicate the disease warrants an exploration of novel vaccine compositions.
Topics: Alleles; Bacterial Outer Membrane Proteins; Biodiversity; Bordetella pertussis; DNA Transposable Elements; Genes, Bacterial; Genetic Variation; Humans; Japan; Pertussis Vaccine; Phylogeny; Polymorphism, Single Nucleotide; Population Dynamics; Sequence Deletion; Vaccines, Acellular; Virulence Factors, Bordetella; Whole Genome Sequencing
PubMed: 29771235
DOI: 10.1099/mgen.0.000180 -
Microbiology and Immunology Nov 2017Culture supernatants of Bordetella pertussis are a brilliant yellow; however, the structure and biological role of the responsible pigment have not been investigated. In...
Culture supernatants of Bordetella pertussis are a brilliant yellow; however, the structure and biological role of the responsible pigment have not been investigated. In this study, a brilliant yellow-colored fraction was extracted from culture supernatants of B. pertussis and analyzed by HPLC. UV-visible spectral analysis and mass spectrometry identified the brilliant yellow pigment as riboflavin. Riboflavin production was high in lag and early log phases and riboflavin was found to enhance growth of B. pertussis in low-density cultures. Riboflavin production is not regulated by the BvgAS system. In addition, it was found that other Bordetella species, such as B. parapertussis, B. holmesii and B. bronchiseptica, also release riboflavin into their culture supernatants. This is the first report that B. pertussis secrets riboflavin to the extracellular space and that riboflavin may promote its growth. The mechanism may be associated with pathogenesis of B. pertussis.
Topics: Bordetella pertussis; Chromatography, High Pressure Liquid; Mass Spectrometry; Pigments, Biological; Riboflavin
PubMed: 28906022
DOI: 10.1111/1348-0421.12541