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      Characterization of Lung and Oral Microbiomes in Lung Cancer Patients Using Culturomics and 16S rRNA Gene Sequencing

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          ABSTRACT

          Recently, microbiota dysbiosis in lung cancer has attracted immense attention. Studies on lung microbes are mostly based on sequencing, which has left the potentially functional bacteria with extremely low abundance uncovered. In this study, we characterized and compared the lung and oral cavity microbiotas using culturomics and 16S rRNA gene sequencing. Of the 198 bacteria identified at the species level from bronchoalveolar lavage fluid (BALF) samples, Firmicutes was predominant (39.90%). Twenty bacterial species isolated from BALF samples were present in at least half of the patients and were also highly abundant in oral samples. Of all isolated strains, Streptococcus and Veillonella were highly dominant. The abundance of Prevotella and Veillonella decreased from the oral cavity to the lung, whereas that of Pseudomonas increased. Linear discriminant analysis effect size demonstrated that Prevotella was more abundant in the healthy samples than in the cancerous ones, which is in accordance with the isolation of Prevotella oralis only from the healthy group using culturomics. Moreover, Gemella sanguinis and Streptococcus intermedius were isolated only from the non-small-cell lung cancer (NSCLC) group, and 16S rRNA gene sequencing showed that they were higher in the NSCLC than in the small-cell lung cancer group. Furthermore, while Bacillus and Castellaniella were enriched in lung adenocarcinoma, Brucella was enriched in lung squamous cell carcinoma. Overall, alterations were observed in the microbial community of patients with lung cancer, whose diversity might be site and pathology dependent. Using culturomics and 16S rRNA gene amplicon sequencing, this study has provided insights into pulmonary and oral microbiota alterations in patients with lung cancer.

          IMPORTANCE The relationship between lung microbiota and cancer has been explored based on DNA sequencing; however, culture-dependent approaches are indispensable for further studies on the lung microbiota. In this study, we applied a comprehensive approach combining culturomics and 16S rRNA gene amplicon sequencing to detect members of the microbiotas in saliva and BALF samples from patients with unilateral lobar masses. We found alterations in the microbial community of patients with lung cancer, whose diversity might be site and pathology dependent. These features may be potential bacterial biomarkers and new targets for lung cancer diagnosis and treatment. In addition, a lung and oral microbial biobank from lung cancer patients was established, which represents a useful resource for studies of host-microbe interactions.

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          Most cited references55

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          Hallmarks of Cancer: New Dimensions

          The hallmarks of cancer conceptualization is a heuristic tool for distilling the vast complexity of cancer phenotypes and genotypes into a provisional set of underlying principles. As knowledge of cancer mechanisms has progressed, other facets of the disease have emerged as potential refinements. Herein, the prospect is raised that phenotypic plasticity and disrupted differentiation is a discrete hallmark capability, and that nonmutational epigenetic reprogramming and polymorphic microbiomes both constitute distinctive enabling characteristics that facilitate the acquisition of hallmark capabilities. Additionally, senescent cells, of varying origins, may be added to the roster of functionally important cell types in the tumor microenvironment. SIGNIFICANCE: Cancer is daunting in the breadth and scope of its diversity, spanning genetics, cell and tissue biology, pathology, and response to therapy. Ever more powerful experimental and computational tools and technologies are providing an avalanche of "big data" about the myriad manifestations of the diseases that cancer encompasses. The integrative concept embodied in the hallmarks of cancer is helping to distill this complexity into an increasingly logical science, and the provisional new dimensions presented in this perspective may add value to that endeavor, to more fully understand mechanisms of cancer development and malignant progression, and apply that knowledge to cancer medicine.
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            Alternative projections of mortality and disability by cause 1990–2020: Global Burden of Disease Study

            The Lancet, 349(9064), 1498-1504
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              Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes.

              Advancement of DNA sequencing technology allows the routine use of genome sequences in the various fields of microbiology. The information held in genome sequences proved to provide objective and reliable means in the taxonomy of prokaryotes. Here, we describe the minimal standards for the quality of genome sequences and how they can be applied for taxonomic purposes.
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                Author and article information

                Contributors
                Role: Editor
                Role: ad hoc peer reviewer
                Role: ad hoc peer reviewer
                Role: ad hoc peer reviewer
                Role: ad hoc peer reviewer
                Journal
                Microbiol Spectr
                Microbiol Spectr
                spectrum
                Microbiology Spectrum
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2165-0497
                24 April 2023
                May-Jun 2023
                24 April 2023
                : 11
                : 3
                : e00314-23
                Affiliations
                [a ] State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China
                [b ] Department of Thoracic Oncology, Peking University Cancer Hospital, Beijing, China
                Chengdu University
                Vellore Institute of Technology University
                Stredoevropsky technologicky institut
                University of Nantes
                Universidad Señor de Sipán
                Author notes

                Yifan Sun and Yuejiao Liu contributed equally to this work. Author order was determined by the corresponding author after negotiation.

                The authors declare no conflict of interest.

                Author information
                https://orcid.org/0000-0002-8309-2259
                https://orcid.org/0000-0001-7600-0734
                https://orcid.org/0000-0002-7105-0940
                Article
                00314-23 spectrum.00314-23
                10.1128/spectrum.00314-23
                10269771
                37092999
                be0f0ac2-359c-49f0-9925-3d2fbe586ecc
                Copyright © 2023 Sun et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 19 January 2023
                : 3 April 2023
                Page count
                supplementary-material: 0, Figures: 5, Tables: 2, Equations: 0, References: 54, Pages: 12, Words: 7712
                Categories
                Research Article
                open-peer-review, Open Peer Review
                microbial-pathogenesis, Microbial Pathogenesis
                Custom metadata
                May/June 2023

                microbiota,lung cancer,balf,oral bacteria,culturomics,16s rrna gene,dna sequencing,lung infection,oral microbiota

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