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

Abstract

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.

The IMPB RAS is 50 years old. Bioinformatics Laboratory

“…Созданы и инкорпорированы в общий программный комплекс 64bit консольные вычислители, анализирующих наличие уникальных относительно совокупности мишеней коротких олигонуклеотидов (kмеров, k = 16, 18, 20 или 22), в геномах E. coli и двух модельных бактерий, чтобы определить, какие из них преимущественно секретируются E. coli в ответ на присутствие другой бактерии. Это позволило выявить потенциально активные внеклеточные РНК и впервые продемонстрировать способность их синтетических аналогов проникать в клетки E. coli и влиять на их рост [28].…”

Sense and antisense RNA products of the uxuR gene can affect motility and chemotaxis acting independent of the UxuR protein

“…Although non-coding transcripts have already been studied for quite a long time, their new biotypes (Markelova et al, 2021;Diallo et al, 2022) and ways of functioning (Hör et al, 2020) are still being discovered. The ability of such transcripts to form duplexes with mRNA allows them to affect almost all stages of gene expression, from transcription and translation to RNA degradation.…”

“…More recently, regulatory functions were described for the fragments originating from tRNAs (tRFs) and the 3′-ends of mRNAs (Lalaouna et al, 2015;Miyakoshi et al, 2015;Chao and Vogel, 2016). Very intriguing are extracellular RNAs (exoRNAs), with a potential to sense and to transmit environmental changes (Ghosal et al, 2015;Alikina et al, 2018;Markelova et al, 2021), and even to mimic eukaryotic microRNAs thus targeting host immune response (Sahr et al, 2022).…”

Rocket-miR, a Translational Launchpad for miRNA-based Antimicrobial Drug Development

“…Conversely, other studies have utilized human and plant-derived miRNAs to enhance the growth or metabolite production of commensal gut bacteria and ameliorate disease symptoms. Furthermore, it is known that bacteria are capable of releasing small RNAs that influence protein expression in other bacteria (45), human cells (46,47), or plant cells (48)(49)(50).…”