The Fate and Functionality of Alien tRNA Fragments in Culturing Medium and Cells of Escherichia coli

Author:

Shavkunov Konstantin S.1,Markelova Natalia Yu.1ORCID,Glazunova Olga A.1,Kolzhetsov Nikolay P.1,Panyukov Valery V.2,Ozoline Olga N.1

Affiliation:

1. Department of Functional Genomics of Prokaryotes, Institute of Cell Biophysics of the Russian Academy of Sciences, Federal Research Center Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences, 142290 Pushchino, Russia

2. Institute of Mathematical Problems of Biology RAS—The Branch of Keldysh Institute of Applied Mathematics of the Russian Academy of Sciences, 142290 Pushchino, Russia

Abstract

Numerous observations have supported the idea that various types of noncoding RNAs, including tRNA fragments (tRFs), are involved in communications between the host and its microbial community. The possibility of using their signaling function has stimulated the study of secreted RNAs, potentially involved in the interspecies interaction of bacteria. This work aimed at identifying such RNAs and characterizing their maturation during transport. We applied an approach that allowed us to detect oligoribonucleotides secreted by Prevotella copri (Segatella copri) or Rhodospirillum rubrum inside Escherichia coli cells. Four tRFs imported by E. coli cells co-cultured with these bacteria were obtained via chemical synthesis, and all of them affected the growth of E. coli. Their successive modifications in the culture medium and recipient cells were studied by high-throughput cDNA sequencing. Instead of the expected accidental exonucleolysis, in the milieu, we observed nonrandom cleavage by endonucleases continued in recipient cells. We also found intramolecular rearrangements of synthetic oligonucleotides, which may be considered traces of intermediate RNA circular isomerization. Using custom software, we estimated the frequency of such events in transcriptomes and secretomes of E. coli and observed surprising reproducibility in positions of such rare events, assuming the functionality of ring isoforms or their permuted derivatives in bacteria.

Funder

Russian Science Foundation

Publisher

MDPI AG

Subject

Inorganic Chemistry,Organic Chemistry,Physical and Theoretical Chemistry,Computer Science Applications,Spectroscopy,Molecular Biology,General Medicine,Catalysis

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1. Special Issue “Bioinformatics of Unusual DNA and RNA Structures”;International Journal of Molecular Sciences;2024-05-10

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