Cargando…

Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria

With the discovery of secreted RNAs, it has become apparent that the biological role of regulatory oligonucleotides likely goes beyond the borders of individual cells. However, the mechanisms of their action are still comprehended only in general terms and mainly for eukaryotic microRNAs, which can...

Descripción completa

Detalles Bibliográficos
Autores principales: Markelova, Natalia, Glazunova, Olga, Alikina, Olga, Panyukov, Valeriy, Shavkunov, Konstantin, Ozoline, Olga
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082180/
https://www.ncbi.nlm.nih.gov/pubmed/33937321
http://dx.doi.org/10.3389/fmolb.2021.609979
_version_ 1783685798114099200
author Markelova, Natalia
Glazunova, Olga
Alikina, Olga
Panyukov, Valeriy
Shavkunov, Konstantin
Ozoline, Olga
author_facet Markelova, Natalia
Glazunova, Olga
Alikina, Olga
Panyukov, Valeriy
Shavkunov, Konstantin
Ozoline, Olga
author_sort Markelova, Natalia
collection PubMed
description With the discovery of secreted RNAs, it has become apparent that the biological role of regulatory oligonucleotides likely goes beyond the borders of individual cells. However, the mechanisms of their action are still comprehended only in general terms and mainly for eukaryotic microRNAs, which can interfere with mRNAs even in distant recipient cells. It has recently become clear that bacterial cells lacking interference systems can also respond to eukaryotic microRNAs that have targets in their genomes. However, the question of whether bacteria can perceive information transmitted by oligonucleotides secreted by other prokaryotes remained open. Here we evaluated the fraction of short RNAs secreted by Escherichia coli during individual and mixed growth with Rhodospirillum rubrum or Prevotella copri, and found that in the presence of other bacteria E. coli tends to excrete oligonucleotides homologous to alien genomes. Based on this observation, we selected four RNAs secreted by either R. rubrum or P. copri, together with one E. coli-specific oligonucleotide. Both fragments of R. rubrum 23S-RNA suppressed the growth of E. coli. Of the two fragments secreted by P. copri, one abolished the stimulatory effect of E. coli RNA derived from the 3′-UTR of ProA mRNA, while the other inhibited bacterial growth only in the double-stranded state with complementary RNA. The ability of two RNAs secreted by cohabiting bacteria to enter E. coli cells was demonstrated using confocal microscopy. Since selected E. coli-specific RNA also affected the growth of this bacterium, we conclude that bacterial RNAs can participate in inter- and intraspecies signaling.
format Online
Article
Text
id pubmed-8082180
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-80821802021-04-30 Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria Markelova, Natalia Glazunova, Olga Alikina, Olga Panyukov, Valeriy Shavkunov, Konstantin Ozoline, Olga Front Mol Biosci Molecular Biosciences With the discovery of secreted RNAs, it has become apparent that the biological role of regulatory oligonucleotides likely goes beyond the borders of individual cells. However, the mechanisms of their action are still comprehended only in general terms and mainly for eukaryotic microRNAs, which can interfere with mRNAs even in distant recipient cells. It has recently become clear that bacterial cells lacking interference systems can also respond to eukaryotic microRNAs that have targets in their genomes. However, the question of whether bacteria can perceive information transmitted by oligonucleotides secreted by other prokaryotes remained open. Here we evaluated the fraction of short RNAs secreted by Escherichia coli during individual and mixed growth with Rhodospirillum rubrum or Prevotella copri, and found that in the presence of other bacteria E. coli tends to excrete oligonucleotides homologous to alien genomes. Based on this observation, we selected four RNAs secreted by either R. rubrum or P. copri, together with one E. coli-specific oligonucleotide. Both fragments of R. rubrum 23S-RNA suppressed the growth of E. coli. Of the two fragments secreted by P. copri, one abolished the stimulatory effect of E. coli RNA derived from the 3′-UTR of ProA mRNA, while the other inhibited bacterial growth only in the double-stranded state with complementary RNA. The ability of two RNAs secreted by cohabiting bacteria to enter E. coli cells was demonstrated using confocal microscopy. Since selected E. coli-specific RNA also affected the growth of this bacterium, we conclude that bacterial RNAs can participate in inter- and intraspecies signaling. Frontiers Media S.A. 2021-04-15 /pmc/articles/PMC8082180/ /pubmed/33937321 http://dx.doi.org/10.3389/fmolb.2021.609979 Text en Copyright © 2021 Markelova, Glazunova, Alikina, Panyukov, Shavkunov and Ozoline. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Biosciences
Markelova, Natalia
Glazunova, Olga
Alikina, Olga
Panyukov, Valeriy
Shavkunov, Konstantin
Ozoline, Olga
Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria
title Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria
title_full Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria
title_fullStr Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria
title_full_unstemmed Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria
title_short Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria
title_sort suppression of escherichia coli growth dynamics via rnas secreted by competing bacteria
topic Molecular Biosciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082180/
https://www.ncbi.nlm.nih.gov/pubmed/33937321
http://dx.doi.org/10.3389/fmolb.2021.609979
work_keys_str_mv AT markelovanatalia suppressionofescherichiacoligrowthdynamicsviarnassecretedbycompetingbacteria
AT glazunovaolga suppressionofescherichiacoligrowthdynamicsviarnassecretedbycompetingbacteria
AT alikinaolga suppressionofescherichiacoligrowthdynamicsviarnassecretedbycompetingbacteria
AT panyukovvaleriy suppressionofescherichiacoligrowthdynamicsviarnassecretedbycompetingbacteria
AT shavkunovkonstantin suppressionofescherichiacoligrowthdynamicsviarnassecretedbycompetingbacteria
AT ozolineolga suppressionofescherichiacoligrowthdynamicsviarnassecretedbycompetingbacteria