Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species
ABSTRACTArginine catabolism by the bacterial arginine deiminase system (ADS) has anticariogenic properties through the production of ammonia, which modulates the pH of the oral environment. Given the potential protective capacity of the ADS pathway, the exploitation of ADS-competent oral microbes th...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-04-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01445-23 |
| _version_ | 1797228822110666752 |
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| author | Allison E. Mann Brinta Chakraborty Lauren M. O'Connell Marcelle M. Nascimento Robert A. Burne Vincent P. Richards |
| author_facet | Allison E. Mann Brinta Chakraborty Lauren M. O'Connell Marcelle M. Nascimento Robert A. Burne Vincent P. Richards |
| author_sort | Allison E. Mann |
| collection | DOAJ |
| description | ABSTRACTArginine catabolism by the bacterial arginine deiminase system (ADS) has anticariogenic properties through the production of ammonia, which modulates the pH of the oral environment. Given the potential protective capacity of the ADS pathway, the exploitation of ADS-competent oral microbes through pre- or probiotic applications is a promising therapeutic target to prevent tooth decay. To date, most investigations of the ADS in the oral cavity and its relation to caries have focused on indirect measures of activity or on specific bacterial groups, yet the pervasiveness and rate of expression of the ADS operon in diverse mixed microbial communities in oral health and disease remain an open question. Here, we use a multivariate approach, combining ultra-deep metatranscriptomic sequencing with paired metataxonomic and in vitro citrulline quantification to characterize the microbial community and ADS operon expression in healthy and late-stage cavitated teeth. While ADS activity is higher in healthy teeth, we identify multiple bacterial lineages with upregulated ADS activity on cavitated teeth that are distinct from those found on healthy teeth using both reference-based mapping and de novo assembly methods. Our dual metataxonomic and metatranscriptomic approach demonstrates the importance of species abundance for gene expression data interpretation and that patterns of differential expression can be skewed by low-abundance groups. Finally, we identify several potential candidate probiotic bacterial lineages within species that may be useful therapeutic targets for the prevention of tooth decay and propose that the development of a strain-specific, mixed-microbial probiotic may be a beneficial approach given the heterogeneity of taxa identified here across health groups.IMPORTANCETooth decay is the most common preventable chronic disease, affecting more than two billion people globally. The development of caries on teeth is primarily a consequence of acid production by cariogenic bacteria that inhabit the plaque microbiome. Other bacterial strains in the oral cavity may suppress or prevent tooth decay by producing ammonia as a byproduct of the arginine deiminase metabolic pathway, increasing the pH of the plaque biofilm. While the benefits of arginine metabolism on oral health have been extensively documented in specific bacterial groups, the prevalence and consistency of arginine deiminase system (ADS) activity among oral bacteria in a community context remain an open question. In the current study, we use a multi-omics approach to document the pervasiveness of the expression of the ADS operon in both health and disease to better understand the conditions in which ADS activity may prevent tooth decay. |
| first_indexed | 2024-04-24T15:02:48Z |
| format | Article |
| id | doaj.art-1c8e42489e5e4f7e999de7b2c95a0acc |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-24T15:02:48Z |
| publishDate | 2024-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-1c8e42489e5e4f7e999de7b2c95a0acc2024-04-02T14:16:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-04-0112410.1128/spectrum.01445-23Heterogeneous lineage-specific arginine deiminase expression within dental microbiome speciesAllison E. Mann0Brinta Chakraborty1Lauren M. O'Connell2Marcelle M. Nascimento3Robert A. Burne4Vincent P. Richards5Department of Biological Sciences, Clemson University, Clemson, South Carolina, USADepartment of Oral Biology, College of Dentistry, University of Florida, Gainesville, Florida, USADepartment of Biological Sciences, Clemson University, Clemson, South Carolina, USADivision of Operative Dentistry, Department of Restorative Dental Sciences, College of Dentistry, University of Florida, Gainesville, Florida, USADepartment of Oral Biology, College of Dentistry, University of Florida, Gainesville, Florida, USADepartment of Biological Sciences, Clemson University, Clemson, South Carolina, USAABSTRACTArginine catabolism by the bacterial arginine deiminase system (ADS) has anticariogenic properties through the production of ammonia, which modulates the pH of the oral environment. Given the potential protective capacity of the ADS pathway, the exploitation of ADS-competent oral microbes through pre- or probiotic applications is a promising therapeutic target to prevent tooth decay. To date, most investigations of the ADS in the oral cavity and its relation to caries have focused on indirect measures of activity or on specific bacterial groups, yet the pervasiveness and rate of expression of the ADS operon in diverse mixed microbial communities in oral health and disease remain an open question. Here, we use a multivariate approach, combining ultra-deep metatranscriptomic sequencing with paired metataxonomic and in vitro citrulline quantification to characterize the microbial community and ADS operon expression in healthy and late-stage cavitated teeth. While ADS activity is higher in healthy teeth, we identify multiple bacterial lineages with upregulated ADS activity on cavitated teeth that are distinct from those found on healthy teeth using both reference-based mapping and de novo assembly methods. Our dual metataxonomic and metatranscriptomic approach demonstrates the importance of species abundance for gene expression data interpretation and that patterns of differential expression can be skewed by low-abundance groups. Finally, we identify several potential candidate probiotic bacterial lineages within species that may be useful therapeutic targets for the prevention of tooth decay and propose that the development of a strain-specific, mixed-microbial probiotic may be a beneficial approach given the heterogeneity of taxa identified here across health groups.IMPORTANCETooth decay is the most common preventable chronic disease, affecting more than two billion people globally. The development of caries on teeth is primarily a consequence of acid production by cariogenic bacteria that inhabit the plaque microbiome. Other bacterial strains in the oral cavity may suppress or prevent tooth decay by producing ammonia as a byproduct of the arginine deiminase metabolic pathway, increasing the pH of the plaque biofilm. While the benefits of arginine metabolism on oral health have been extensively documented in specific bacterial groups, the prevalence and consistency of arginine deiminase system (ADS) activity among oral bacteria in a community context remain an open question. In the current study, we use a multi-omics approach to document the pervasiveness of the expression of the ADS operon in both health and disease to better understand the conditions in which ADS activity may prevent tooth decay.https://journals.asm.org/doi/10.1128/spectrum.01445-23metatranscriptomicsarginine deiminase systemprobioticsoral microbiomecaries |
| spellingShingle | Allison E. Mann Brinta Chakraborty Lauren M. O'Connell Marcelle M. Nascimento Robert A. Burne Vincent P. Richards Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species Microbiology Spectrum metatranscriptomics arginine deiminase system probiotics oral microbiome caries |
| title | Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species |
| title_full | Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species |
| title_fullStr | Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species |
| title_full_unstemmed | Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species |
| title_short | Heterogeneous lineage-specific arginine deiminase expression within dental microbiome species |
| title_sort | heterogeneous lineage specific arginine deiminase expression within dental microbiome species |
| topic | metatranscriptomics arginine deiminase system probiotics oral microbiome caries |
| url | https://journals.asm.org/doi/10.1128/spectrum.01445-23 |
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