The oral microbiome is one of the most complex microbial communities in the human body, and due to circumstances not completely understood, the healthy microbial community becomes dysbiotic, giving rise to periodontitis, a polymicrobial inflammatory disease. We previously reported the results of community-wide gene expression changes in the oral microbiome during periodontitis progression and identified signatures associated with increasing severity of the disease. Small noncoding RNAs (sRNAs) are key players in posttranscriptional regulation, especially in fast-changing environments such as the oral cavity. Here, we expanded our analysis to the study of the sRNA metatranscriptome during periodontitis progression on the same samples for which mRNA expression changes were analyzed. We observed differential expression of 12,097 sRNAs, identifying a total of 20 Rfam sRNA families as being overrepresented in progression and 23 at baseline. Gene ontology activities regulated by the differentially expressed (DE) sRNAs included amino acid metabolism, ethanolamine catabolism, signal recognition particle-dependent cotranslational protein targeting to membrane, intron splicing, carbohydrate metabolism, control of plasmid copy number, and response to stress. In integrating patterns of expression of protein coding transcripts and sRNAs, we found that functional activities of genes that correlated positively with profiles of expression of DE sRNAs were involved in pathogenesis, proteolysis, ferrous iron transport, and oligopeptide transport. These findings represent the first integrated sequencing analysis of the community-wide sRNA transcriptome of the oral microbiome during periodontitis progression and show that sRNAs are key regulatory elements of the dysbiotic process leading to disease.
Bacterial small noncoding RNAs (sRNAs) encompass a large and diverse group of RNA molecules that do not result in the translation of a protein product. They show high heterogeneity in size and structure and many are used in regulatory roles or other functional capacities upon transcription. sRNAs are important in bacteria because they can be used to adapt rapidly to changing environmental conditions, especially in an environment such as the oral cavity, which is exposed daily to regular changes in amount and quality of nutrients available for use by the oral biofilms. Most of these sRNAs are encoded in the 5= and 3= untranslated regions, as well as in intergenic regions (IGRs) of the genome (1).sRNAs display a wide variety of mechanisms of action. sRNAs repress translation of mRNA by attaching to the ribosome binding site (RBS) competing with the ribosome and leading to the rapid degradation of the mRNA (2). Other noncanonical mechanisms of translation repression have been also described, such as binding cis-acting antisense RNA to a ribosome standby site upstream of the RBS (3). In addition, sRNAs can also activate the translations of mRNAs (4, 5) or can modulate gene expression by varying the level of transcript stability (6). sRNA ca...