Comparison of qPCR protocols for quantification of “Candidatus Saccharibacteria”, belonging to the Candidate Phyla Radiation, suggests that 23S rRNA is a better target than 16S rRNA

Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disor...

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Published inPloS one Vol. 19; no. 12; p. e0310675
Main Authors Papaleo, Stella, Nodari, Riccardo, Sterzi, Lodovico, D’Auria, Enza, Cattaneo, Camilla, Bettoni, Giorgia, Bonaiti, Clara, Pagliarini, Ella, Zuccotti, Gianvincenzo, Panelli, Simona, Comandatore, Francesco
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 26.12.2024
Public Library of Science (PLoS)
Subjects
Bacteria
Biology and life sciences
Comparative analysis
Computer and Information Sciences
Datasets
Deoxyribonucleic acid
DNA
DNA sequencing
DNA, Bacterial - genetics
Experiments
Gene sequencing
Genes
Genetic analysis
Genetic testing
Genetic variability
Genomes
Humans
Identification and classification
Immunomodulation
Medicine and Health Sciences
Microbiota
Microbiota - genetics
Microorganisms
Phylogenetics
Phylogeny
Polymerase chain reaction
Primers
Radiation
Real-Time Polymerase Chain Reaction - methods
Research and Analysis Methods
Ribosomal RNA
RNA, Ribosomal, 16S - genetics
RNA, Ribosomal, 23S - genetics
rRNA 16S
rRNA 23S
Saccharibacteria
Saliva
Saliva - microbiology
Taxonomy
Tumor necrosis factor-TNF
Varieties
Italy
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Abstract Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva. Four qPCR protocols for quantifying "Ca. Saccharibacteria" (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the "Ca. Saccharibacteria" genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated "Ca. Saccharibacteria" in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing. Overall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying "Ca. Saccharibacteria", although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying "Ca. Saccharibacteria", highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of "Ca. Saccharibacteria" in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
AbstractList Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva. Four qPCR protocols for quantifying "Ca. Saccharibacteria" (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the "Ca. Saccharibacteria" genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated "Ca. Saccharibacteria" in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing. Overall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying "Ca. Saccharibacteria", although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying "Ca. Saccharibacteria", highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of "Ca. Saccharibacteria" in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
BackgroundCandidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, “Candidatus Saccharibacteria” is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva.Methods and resultsFour qPCR protocols for quantifying “Ca. Saccharibacteria” (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the “Ca. Saccharibacteria” genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated “Ca. Saccharibacteria” in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing.ConclusionOverall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying “Ca. Saccharibacteria”, although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying “Ca. Saccharibacteria”, highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of “Ca. Saccharibacteria” in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
Background Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva. Methods and results Four qPCR protocols for quantifying "Ca. Saccharibacteria" (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the "Ca. Saccharibacteria" genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated "Ca. Saccharibacteria" in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing. Conclusion Overall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying "Ca. Saccharibacteria", although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying "Ca. Saccharibacteria", highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of "Ca. Saccharibacteria" in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva. Four qPCR protocols for quantifying "Ca. Saccharibacteria" (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the "Ca. Saccharibacteria" genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated "Ca. Saccharibacteria" in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing. Overall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying "Ca. Saccharibacteria", although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying "Ca. Saccharibacteria", highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of "Ca. Saccharibacteria" in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
Background Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, “ Candidatus Saccharibacteria” is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva. Methods and results Four qPCR protocols for quantifying “ Ca . Saccharibacteria” (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the “ Ca . Saccharibacteria” genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated “ Ca . Saccharibacteria” in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing. Conclusion Overall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying “ Ca . Saccharibacteria”, although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying “ Ca . Saccharibacteria”, highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of “ Ca . Saccharibacteria” in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva.BACKGROUNDCandidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of the most clinically relevant phyla. Indeed, it is enriched in the oral microbiota of subjects suffering from immune-mediated disorders and it has been found to have immunomodulatory activities. For these reasons, it is crucial to have reliable methods to detect and quantify this bacterial lineage in human samples, including saliva.Four qPCR protocols for quantifying "Ca. Saccharibacteria" (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the "Ca. Saccharibacteria" genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated "Ca. Saccharibacteria" in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing.METHODS AND RESULTSFour qPCR protocols for quantifying "Ca. Saccharibacteria" (one targeting the 23S rRNA gene and three the 16S) were tested and compared. The efficiency and coverage of these four protocols were evaluated in silico on large genomic datasets, and in vitro on salivary DNA samples, already characterized by amplicon sequencing on the V3-V4 regions of the 16S rRNA. In silico PCR analyses showed that all qPCR primers lose part of the "Ca. Saccharibacteria" genetic variability, even if the 23S qPCR primers matched more lineages than the 16S qPCR primers. In vitro qPCR experiments confirmed that all 16S-based protocols strongly underestimated "Ca. Saccharibacteria" in salivary DNA, while the 23S qPCR protocol gave quantifications more comparable to 16S amplicon sequencing.Overall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying "Ca. Saccharibacteria", although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying "Ca. Saccharibacteria", highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of "Ca. Saccharibacteria" in clinical samples could hide its role in human health and in the development of immune-mediated diseases.CONCLUSIONOverall, our results show that the 23S-based qPCR protocol is more precise than the 16S-based ones in quantifying "Ca. Saccharibacteria", although all protocols probably underestimate specific lineages. These results underline the current limits in quantifying "Ca. Saccharibacteria", highlighting the needs for novel experimental strategies or methods. Indeed, the underestimation of "Ca. Saccharibacteria" in clinical samples could hide its role in human health and in the development of immune-mediated diseases.
Audience Academic
Author Bonaiti, Clara
Sterzi, Lodovico
Papaleo, Stella
Bettoni, Giorgia
D’Auria, Enza
Cattaneo, Camilla
Zuccotti, Gianvincenzo
Comandatore, Francesco
Nodari, Riccardo
Pagliarini, Ella
Panelli, Simona
AuthorAffiliation 2 Department of Pediatrics, Buzzi Children’s Hospital, University of Milan, Milan, Italy
South China University of Technology, CHINA
1 Pediatric Clinical Research Center “Invernizzi”, Department of Biomedical and Clinical Sciences, University of Milan, Milan, Italy
3 Sensory & Consumer Science Lab (SCS_Lab), Department of Food, Environmental and Nutritional Sciences, University of Milan, Milan, Italy
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/39724137$$D View this record in MEDLINE/PubMed
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License Copyright: © 2024 Papaleo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Competing Interests: The authors have declared that no competing interests exist.
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Snippet Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria" is one of...
Background Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus...
BackgroundCandidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, “Candidatus Saccharibacteria”...
BackgroundCandidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, "Candidatus Saccharibacteria"...
Background Candidate Phyla Radiation (CPR) is a large monophyletic group encompassing about 25% of bacterial diversity. Among CPR, “ Candidatus...
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SubjectTerms Bacteria
Biology and life sciences
Comparative analysis
Computer and Information Sciences
Datasets
Deoxyribonucleic acid
DNA
DNA sequencing
DNA, Bacterial - genetics
Experiments
Gene sequencing
Genes
Genetic analysis
Genetic testing
Genetic variability
Genomes
Humans
Identification and classification
Immunomodulation
Medicine and Health Sciences
Microbiota
Microbiota - genetics
Microorganisms
Phylogenetics
Phylogeny
Polymerase chain reaction
Primers
Radiation
Real-Time Polymerase Chain Reaction - methods
Research and Analysis Methods
Ribosomal RNA
RNA, Ribosomal, 16S - genetics
RNA, Ribosomal, 23S - genetics
rRNA 16S
rRNA 23S
Saccharibacteria
Saliva
Saliva - microbiology
Taxonomy
Tumor necrosis factor-TNF
Varieties
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Title Comparison of qPCR protocols for quantification of “Candidatus Saccharibacteria”, belonging to the Candidate Phyla Radiation, suggests that 23S rRNA is a better target than 16S rRNA
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