Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications
Viruses are obligate intracellular parasites that, throughout evolution, have adapted numerous strategies to control the translation machinery, including the modulation of post-transcriptional modifications (PTMs) on transfer RNA (tRNA). PTMs are critical translation regulators used to further host...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-01-01
|
| Series: | Microorganisms |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2607/11/2/355 |
| _version_ | 1827756277109882880 |
|---|---|
| author | Mirka Lampi Pavlina Gregorova M. Suleman Qasim Niklas C. V. Ahlblad L. Peter Sarin |
| author_facet | Mirka Lampi Pavlina Gregorova M. Suleman Qasim Niklas C. V. Ahlblad L. Peter Sarin |
| author_sort | Mirka Lampi |
| collection | DOAJ |
| description | Viruses are obligate intracellular parasites that, throughout evolution, have adapted numerous strategies to control the translation machinery, including the modulation of post-transcriptional modifications (PTMs) on transfer RNA (tRNA). PTMs are critical translation regulators used to further host immune responses as well as the expression of viral proteins. Yet, we lack critical insight into the temporal dynamics of infection-induced changes to the tRNA modification landscape (i.e., ‘modificome’). In this study, we provide the first comprehensive quantitative characterization of the tRNA modificome in the marine bacterium <i>Shewanella glacialimarina</i> during Shewanella phage 1/4 infection. Specifically, we show that PTMs can be grouped into distinct categories based on modification level changes at various infection stages. Furthermore, we observe a preference for the UAC codon in viral transcripts expressed at the late stage of infection, which coincides with an increase in queuosine modification. Queuosine appears exclusively on tRNAs with GUN anticodons, suggesting a correlation between phage codon usage and PTM modification. Importantly, this work provides the basis for further studies into RNA-based regulatory mechanisms employed by bacteriophages to control the prokaryotic translation machinery. |
| first_indexed | 2024-03-11T08:22:56Z |
| format | Article |
| id | doaj.art-35d1aad48a26492795cada4c0d5451bf |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-11T08:22:56Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-35d1aad48a26492795cada4c0d5451bf2023-11-16T22:14:43ZengMDPI AGMicroorganisms2076-26072023-01-0111235510.3390/microorganisms11020355Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA ModificationsMirka Lampi0Pavlina Gregorova1M. Suleman Qasim2Niklas C. V. Ahlblad3L. Peter Sarin4RNAcious Laboratory, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, FinlandRNAcious Laboratory, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, FinlandRNAcious Laboratory, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, FinlandRNAcious Laboratory, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, FinlandRNAcious Laboratory, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, FinlandViruses are obligate intracellular parasites that, throughout evolution, have adapted numerous strategies to control the translation machinery, including the modulation of post-transcriptional modifications (PTMs) on transfer RNA (tRNA). PTMs are critical translation regulators used to further host immune responses as well as the expression of viral proteins. Yet, we lack critical insight into the temporal dynamics of infection-induced changes to the tRNA modification landscape (i.e., ‘modificome’). In this study, we provide the first comprehensive quantitative characterization of the tRNA modificome in the marine bacterium <i>Shewanella glacialimarina</i> during Shewanella phage 1/4 infection. Specifically, we show that PTMs can be grouped into distinct categories based on modification level changes at various infection stages. Furthermore, we observe a preference for the UAC codon in viral transcripts expressed at the late stage of infection, which coincides with an increase in queuosine modification. Queuosine appears exclusively on tRNAs with GUN anticodons, suggesting a correlation between phage codon usage and PTM modification. Importantly, this work provides the basis for further studies into RNA-based regulatory mechanisms employed by bacteriophages to control the prokaryotic translation machinery.https://www.mdpi.com/2076-2607/11/2/355host–pathogen interactionpost-transcriptional nucleoside modificationtranslationtransfer RNAShewanella phage 1/4<i>Shewanella glacialimarina</i> |
| spellingShingle | Mirka Lampi Pavlina Gregorova M. Suleman Qasim Niklas C. V. Ahlblad L. Peter Sarin Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications Microorganisms host–pathogen interaction post-transcriptional nucleoside modification translation transfer RNA Shewanella phage 1/4 <i>Shewanella glacialimarina</i> |
| title | Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications |
| title_full | Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications |
| title_fullStr | Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications |
| title_full_unstemmed | Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications |
| title_short | Bacteriophage Infection of the Marine Bacterium <i>Shewanella glacialimarina</i> Induces Dynamic Changes in tRNA Modifications |
| title_sort | bacteriophage infection of the marine bacterium i shewanella glacialimarina i induces dynamic changes in trna modifications |
| topic | host–pathogen interaction post-transcriptional nucleoside modification translation transfer RNA Shewanella phage 1/4 <i>Shewanella glacialimarina</i> |
| url | https://www.mdpi.com/2076-2607/11/2/355 |
| work_keys_str_mv | AT mirkalampi bacteriophageinfectionofthemarinebacteriumishewanellaglacialimarinaiinducesdynamicchangesintrnamodifications AT pavlinagregorova bacteriophageinfectionofthemarinebacteriumishewanellaglacialimarinaiinducesdynamicchangesintrnamodifications AT msulemanqasim bacteriophageinfectionofthemarinebacteriumishewanellaglacialimarinaiinducesdynamicchangesintrnamodifications AT niklascvahlblad bacteriophageinfectionofthemarinebacteriumishewanellaglacialimarinaiinducesdynamicchangesintrnamodifications AT lpetersarin bacteriophageinfectionofthemarinebacteriumishewanellaglacialimarinaiinducesdynamicchangesintrnamodifications |