Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community

ABSTRACT Regulatory small RNAs (sRNAs) play large-scale and essential roles in many cellular processes across all domains of life. Microbial sRNAs have been extensively studied in model organisms, but very little is known about the dynamics of sRNA synthesis and their roles in the natural environmen...

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Main Authors: Diego R. Gelsinger, Gherman Uritskiy, Rahul Reddy, Adam Munn, Katie Farney, Jocelyne DiRuggiero
Format: Article
Language:English
Published: American Society for Microbiology 2020-02-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mSystems.00584-19
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author Diego R. Gelsinger
Gherman Uritskiy
Rahul Reddy
Adam Munn
Katie Farney
Jocelyne DiRuggiero
author_facet Diego R. Gelsinger
Gherman Uritskiy
Rahul Reddy
Adam Munn
Katie Farney
Jocelyne DiRuggiero
author_sort Diego R. Gelsinger
collection DOAJ
description ABSTRACT Regulatory small RNAs (sRNAs) play large-scale and essential roles in many cellular processes across all domains of life. Microbial sRNAs have been extensively studied in model organisms, but very little is known about the dynamics of sRNA synthesis and their roles in the natural environment. In this study, we discovered hundreds of intergenic (itsRNAs) and antisense (asRNAs) sRNAs expressed in an extremophilic microbial community inhabiting halite nodules (salt rocks) in the Atacama Desert. For this, we built SnapT, a new sRNA annotation pipeline that can be applied to any microbial community. We found asRNAs with expression levels negatively correlated with that of their overlapping putative target and itsRNAs that were conserved and significantly differentially expressed between 2 sampling time points. We demonstrated that we could perform target prediction and correlate expression levels between sRNAs and predicted target mRNAs at the community level. Functions of putative mRNA targets reflected the environmental challenges members of the halite communities were subjected to, including osmotic adjustments to a major rain event and competition for nutrients. IMPORTANCE Microorganisms in the natural world are found in communities, communicating and interacting with each other; therefore, it is essential that microbial regulatory mechanisms, such as gene regulation affected by small RNAs (sRNAs), be investigated at the community level. This work demonstrates that metatranscriptomic field experiments can link environmental variation with changes in RNA pools and have the potential to provide new insights into environmental sensing and responses in natural microbial communities through noncoding RNA-mediated gene regulation.
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spelling doaj.art-454f692b70ab473c98167d3d1f931d932022-12-21T21:24:31ZengAmerican Society for MicrobiologymSystems2379-50772020-02-015110.1128/mSystems.00584-19Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial CommunityDiego R. Gelsinger0Gherman Uritskiy1Rahul Reddy2Adam Munn3Katie Farney4Jocelyne DiRuggiero5Department of Biology, The Johns Hopkins University, Baltimore, Maryland, USADepartment of Biology, The Johns Hopkins University, Baltimore, Maryland, USADepartment of Biology, The Johns Hopkins University, Baltimore, Maryland, USADepartment of Biology, The Johns Hopkins University, Baltimore, Maryland, USADepartment of Biology, The Johns Hopkins University, Baltimore, Maryland, USADepartment of Biology, The Johns Hopkins University, Baltimore, Maryland, USAABSTRACT Regulatory small RNAs (sRNAs) play large-scale and essential roles in many cellular processes across all domains of life. Microbial sRNAs have been extensively studied in model organisms, but very little is known about the dynamics of sRNA synthesis and their roles in the natural environment. In this study, we discovered hundreds of intergenic (itsRNAs) and antisense (asRNAs) sRNAs expressed in an extremophilic microbial community inhabiting halite nodules (salt rocks) in the Atacama Desert. For this, we built SnapT, a new sRNA annotation pipeline that can be applied to any microbial community. We found asRNAs with expression levels negatively correlated with that of their overlapping putative target and itsRNAs that were conserved and significantly differentially expressed between 2 sampling time points. We demonstrated that we could perform target prediction and correlate expression levels between sRNAs and predicted target mRNAs at the community level. Functions of putative mRNA targets reflected the environmental challenges members of the halite communities were subjected to, including osmotic adjustments to a major rain event and competition for nutrients. IMPORTANCE Microorganisms in the natural world are found in communities, communicating and interacting with each other; therefore, it is essential that microbial regulatory mechanisms, such as gene regulation affected by small RNAs (sRNAs), be investigated at the community level. This work demonstrates that metatranscriptomic field experiments can link environmental variation with changes in RNA pools and have the potential to provide new insights into environmental sensing and responses in natural microbial communities through noncoding RNA-mediated gene regulation.https://journals.asm.org/doi/10.1128/mSystems.00584-19RNAextremophilesgene regulationmetagenomicsmetatranscriptomicsmicrobial communities
spellingShingle Diego R. Gelsinger
Gherman Uritskiy
Rahul Reddy
Adam Munn
Katie Farney
Jocelyne DiRuggiero
Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
mSystems
RNA
extremophiles
gene regulation
metagenomics
metatranscriptomics
microbial communities
title Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
title_full Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
title_fullStr Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
title_full_unstemmed Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
title_short Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community
title_sort regulatory noncoding small rnas are diverse and abundant in an extremophilic microbial community
topic RNA
extremophiles
gene regulation
metagenomics
metatranscriptomics
microbial communities
url https://journals.asm.org/doi/10.1128/mSystems.00584-19
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