Shotgun proteomic analysis of Bordetella parapertussis provides insights into the physiological response to iron starvation and potential new virulence determinants absent in Bordetella pertussis

Oviedo, Juan Marcos; Surmann, Kristin; Gorgojo, Juan Pablo; Valdez, Hugo A.; Dhople, Vishnu M.; Lamberti, Yanina Andrea; Völker, Uwe; Rodrı́guez, Marı́a Eugenia

doi:10.1016/j.jprot.2019.103448

Cited by 5 publications

(9 citation statements)

References 71 publications

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“…Recently, it has been demonstrated that the abundance of filamentous hemagglutinin FhaB, the main adhesin of B. pertussis , as well as fimbrial proteins, adenylate cyclase and pertussis toxins, are affected during iron restriction influencing the first steps of colonization and intracellular infection development [9 ▪ ]. Similar observations were made for the closely related B. parapertussis [42 ▪ ].…”

Section: Iron Availability or Restriction Trigger Host-pathogen Inter...mentioning

confidence: 59%

The intracellular phase of extracellular respiratory tract bacterial pathogens and its role on pathogen-host interactions during infection

Lamberti

Surmann

2021

Current Opinion in Infectious Diseases

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Purpose of review An initial intracellular phase of usually extracellular bacterial pathogens displays an important strategy to hide from the host's immune system and antibiotics therapy. It helps the bacteria, including bacterial pathogens of airway diseases, to persist and eventually switch to a typical extracellular infection. Several infectious diseases of the lung are life-threatening and their control is impeded by intracellular persistence of pathogens. Thus, molecular adaptations of the pathogens to this niche but also the host's response and potential targets to interfere are of relevance. Here we discuss examples of historically considered extracellular pathogens of the respiratory airway where the intracellular survival and proliferation is well documented, including infections by Staphylococcus aureus, Bordetella pertussis, Haemophilus influenzae, Pseudomonas aeruginosa, and others. Recent findings Current studies focus on bacterial factors contributing to adhesion, iron acquisition, and intracellular survival as well as ways to target them for combatting the bacterial infections. Summary The investigation of common and specific mechanisms of pathogenesis and persistence of these bacteria in the host may contribute to future investigations and identifications of relevant factors and/or bacterial mechanisms to be blocked to treat or improve prevention strategies.

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Section: Iron Availability or Restriction Trigger Host-pathogen Inter...mentioning

confidence: 59%

The intracellular phase of extracellular respiratory tract bacterial pathogens and its role on pathogen-host interactions during infection

Lamberti

Surmann

2021

Current Opinion in Infectious Diseases

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“…PetABC is the cytochrome 13 bc complex (complex III) that transfers electrons to cytochrome c (BP3650) and translocates protons across the membrane to create the proton motive force that powers ATP synthase (47). PetABC was found to be upregulated in iron repressed conditions and in low oxygen conditions in other species (48)(49)(50). This suggest that the regulatory pathways that are induced in low iron or oxygen may be triggered in the cluster I strain.…”

Section: Discussionmentioning

confidence: 99%

Proteomic comparison of epidemic AustralianBordetella pertussisbiofilm cells

Suyama,

Luu,

Zhong

et al. 2024

Preprint

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Bordetella pertussiscauses whooping cough, a severe respiratory infectious disease. Studies have compared the currently dominant single nucleotide polymorphism (SNP) cluster I (pertussis toxin promoter allele,ptxP3) and previously dominant SNP cluster II (ptxP1) strains as planktonic cells. Since biofilm formation is linked withB. pertussispathogenesisin vivo, this study compared the biofilm formation capabilities of representative strains of cluster I and cluster II. Confocal laser scanning microscopy found that the cluster I strain had a denser biofilm structure compared to the cluster II strain. Differences in protein expression of the biofilm cells were then compared using Tandem Mass Tagging (TMT) and high-resolution multiple reaction monitoring (MRM-hr). In total, 1453 proteins were identified of which 40 proteins had significant differential expression between the two strains in biofilm conditions. Of particular interest was a large increase in expression of energy metabolism proteins (cytochrome proteins PetABC and BP3650) in the cluster I strain. When the expression of these proteins was compared between 6 additional strains from each cluster, it was found that the protein expression varied between all strains. These findings suggest that there are large levels of individual proteomic diversity betweenB. pertussisstrains in biofilm conditions despite the highly conserved genome of the species. Overall, this study revealed visual differences in biofilm structure betweenB. pertussisstrains and highlighted strain specific variation in protein expression that dominate potential cluster specific changes that may be linked with the dominance of cluster I strains.ImportanceBordetella pertussiscauses whooping cough. The currently circulating cluster I strains have taken over previously dominant cluster II strains. It is important to understand the reasons behind the evolution to develop new strategies against the pathogen. Recent studies have shown thatB. pertussiscan form biofilms during infection. This study compared the biofilm formation capabilities of a cluster I and a cluster II strain and identified visual differences in the biofilms. The protein expression between these strains grown in biofilms were compared and proteins identified with varied expression were measured with additional strains from each cluster. It was found that despite the highly conserved genetics of the species, there was varied protein expression between the additional strains. This study highlights that strain specific variation in protein expression during biofilm conditions that may dominate the cluster specific changes that may be linked to the dominance of cluster I strains.

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“…Finally, we also examined if phosphorylation differences between classical Bordetella species may be due to proteome differences. We compared whether the phosphoproteins identified in this study were detected in the proteomes from previous Bordetella studies ( Kurushima et al, 2012;Luu et al, 2018a; Luu et al, 2018b;Oviedo et al, 2019). Most phosphoproteins (70-75%) identified in one Bordetella species have been previously detected in the proteome of other Bordetella species (Supplementary Table 5).…”

Section: Conservation Of Phosphoproteins and Phosphorylation Sites In Classical Bordetella Speciesmentioning

confidence: 98%

“…There are limited proteomic studies that have compared the proteomes of all three classical Bordetella species. A recent study by Oviedo et al (2019) investigated proteomic differences between B. pertussis and B. parapertussis and identified key expression differences in stress response proteins which may lead to differences in persistence within the host between the two Bordetella pathogens.…”

Section: Introductionmentioning

confidence: 99%

Comparative Phosphoproteomics of Classical Bordetellae Elucidates the Potential Role of Serine, Threonine and Tyrosine Phosphorylation in Bordetella Biology and Virulence

Luu

Zhong

Kaur

et al. 2021

Front. Cell. Infect. Microbiol.

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The Bordetella genus is divided into two groups: classical and non-classical. Bordetella pertussis, Bordetella bronchiseptica and Bordetella parapertussis are known as classical bordetellae, a group of important human pathogens causing whooping cough or whooping cough-like disease and hypothesized to have evolved from environmental non-classical bordetellae. Bordetella infections have increased globally driving the need to better understand these pathogens for the development of new treatments and vaccines. One unexplored component in Bordetella is the role of serine, threonine and tyrosine phosphorylation. Therefore, this study characterized the phosphoproteome of classical bordetellae and examined its potential role in Bordetella biology and virulence. Applying strict identification of localization criteria, this study identified 70 unique phosphorylated proteins in the classical bordetellae group with a high degree of conservation. Phosphorylation was a key regulator of Bordetella metabolism with proteins involved in gluconeogenesis, TCA cycle, amino acid and nucleotide synthesis significantly enriched. Three key virulence pathways were also phosphorylated including type III secretion system, alcaligin synthesis and the BvgAS master transcriptional regulatory system for virulence genes in Bordetella. Seven new phosphosites were identified in BvgA with 6 located in the DNA binding domain. Of the 7, 4 were not present in non-classical bordetellae. This suggests that serine/threonine phosphorylation may play an important role in stabilizing/destabilizing BvgA binding to DNA for fine-tuning of virulence gene expression and that BvgA phosphorylation may be an important factor separating classical from non-classical bordetellae. This study provides the first insight into the phosphoproteome of classical Bordetella species and the role that Ser/Thr/Tyr phosphorylation may play in Bordetella biology and virulence.

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Shotgun proteomic analysis of Bordetella parapertussis provides insights into the physiological response to iron starvation and potential new virulence determinants absent in Bordetella pertussis

Cited by 5 publications

References 71 publications

The intracellular phase of extracellular respiratory tract bacterial pathogens and its role on pathogen-host interactions during infection

The intracellular phase of extracellular respiratory tract bacterial pathogens and its role on pathogen-host interactions during infection

Proteomic comparison of epidemic AustralianBordetella pertussisbiofilm cells

Comparative Phosphoproteomics of Classical Bordetellae Elucidates the Potential Role of Serine, Threonine and Tyrosine Phosphorylation in Bordetella Biology and Virulence

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