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An integrated multi-omic workflow reveals markers of host-microbe dynamics in clinical cystic fibrosis samples

ABSTRACT: Airway microbiota composition correlates with cystic fibrosis (CF) progression, however, microbial drivers of disease remain unclear. MS-based metaproteomics of bronchoalveolar lavage fluid (BALF) offers insights into both host and microbe dynamics and potential interactions. However, detection of microbial proteins, and analysis of their interaction with host proteins is analytically challenging. As a solution, we have developed a novel, integrated workflow coupling deep MS-based BALF analysis, with customized bioinformatic processing of both host and microbial proteins, generating a panel of verified host and microbe peptide candidates suitable for targeted analysis within individual patient samples. We have utilized this workflow in our ongoing work to identify a promising host and microbe peptide panel for application to CF disease progression studies.

INSTRUMENT(S): Orbitrap Eclipse, Orbitrap Fusion

ORGANISM(S): Homo Sapiens (human)

TISSUE(S): Lung, Bronchoalveolar Lavage

DISEASE(S): Cystic Fibrosis

SUBMITTER: Monica Kruk

LAB HEAD: Timothy Griffin

PROVIDER: PXD041457 | Pride | 2024-06-25

REPOSITORIES: Pride

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Dataset's files

Source:

			Action	DRS
	DiscoveryPool_CFH_FlashLFQ_QuantifiedPeaks.tabular	Other
	DiscoveryPool_CFH_PepQuery_PSMRank.tabular	Other
	DiscoveryPool_CFH_SearchGuiPeptideShaker_PSMreport.tabular	Other
	DiscoveryPool_CFL_FlashLFQ_QuantifiedPeaks.tabular	Other
	DiscoveryPool_CFL_PepQuery_PSMRank.tabular	Other

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Project description:Oral health is associated with a symbiotic microbial community and host-microbe homeostasis is maintained by the controlled immune response. Various factors can disrupt this homeostasis. Dysbiosis, which is characterized by increased immune response and a shift in the microbiome, contributes the pathogenesis of peri-implantitis. Peri-implant mucosa and commensal bacteria play important roles in the maintenance of host-microbe homeostasis, but little is known about how they interact. We have therefore investigated the early host-microbe interaction between a commensal multispecies biofilm (Streptococcus oralis, Actinomyces naeslundii, Veillonella dispar, Porphyromonas gingivalis) and peri-implant mucosa at 24 and 48 h. Our in vitro peri-implant mucosa-biofilm model contained organotypic oral mucosa, implant material and biofilm. After 24 h, the biofilm induced a modest innate immune response in the peri-implant mucosa by the upregulation of 5 genes related to immune and inflammatory response and the increased secretion of IL-6 and CCL20. This controlled immune response protected tissue integrity and the peri-implant mucosa remained intact. The secreted antibacterial proteins human β-Defensins-1, -2, and CCL20 controlled the overgrowth of the biofilm by reducing its volume - without affecting the live/dead ratio or bacterial distribution. Thus, host-microbe homeostasis was established within the first 24 h. In contrast, host-microbe homeostasis was disrupted after 48 h. The mucosa was damaged and detached from the implant, due to the induced downregulation of cell adhesion related genes. The immune response was enhanced by upregulation of additional genes related to the immune and inflammatory response and increased secretion of IL-1β, TNF-α, and CCL20. Moreover, bacterial distribution was altered, with an increased proportion of V. dispar. The disrupted host-microbe homeostasis could lead to incipient dysbiosis. This deeper understanding of the early host-microbe interaction at the peri-implant site may provide the basis for new strategies to improve the prevention and therapy of peri-implant diseases.

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An integrated multi-omic workflow reveals markers of host-microbe dynamics in clinical cystic fibrosis samples

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