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Title: The RNA Complement of Outer Membrane Vesicles From Salmonella enterica Serovar Typhimurium Under Distinct Culture Conditions

Abstract

Here, bacterial outer membrane vesicles (OMVs), as well as OMV-associated small RNAs, have been demonstrated to play a role in host–pathogen interactions. The presence of larger RNA transcripts in OMVs has been less studied and their potential role in host–pathogen interactions remains largely unknown. Here we analyze RNA from OMVs secreted by Salmonella enterica serovar Typhimurium (S. Typhimurium) cultured under different conditions, which mimic host–pathogen interactions. S. Typhimurium was grown to exponential and stationary growth phases in minimal growth control medium (phosphate-carbon-nitrogen, PCN), as well as in acidic and phosphate-depleted PCN, comparable to the macrophage environment and inducing therefore the expression of Salmonella pathogenicity island 2 (SPI-2) genes. Moreover, Salmonella pathogenicity island 1 (SPI-1), which is required for virulence during the intestinal phase of infection, was induced by culturing S. Typhimurium to the stationary phase in Lysogeny Broth (LB). For each condition, we identified OMV-associated RNAs that are enriched in the extracellular environment relative to the intracellular space. All RNA classes could be observed, but a vast majority of rRNA was exported in all conditions in variable proportions with a notable decrease in LB SPI-1 inducing media. Several mRNAs and ncRNAs were specifically enriched in/on OMVs dependent on the growthmore » conditions. Important to note is that some RNAs showed identical read coverage profiles intracellularly and extracellularly, whereas distinct coverage patterns were observed for other transcripts, suggesting a specific processing or degradation. Moreover, PCR experiments confirmed that distinct RNAs were present in or on OMVs as full-length transcripts (IsrB-1/2; IsrA; ffs; SsrS; CsrC; pSLT035; 10Sa; rnpB; STM0277; sseB; STM0972; STM2606), whereas others seemed to be rather present in a processed or degraded form. Finally, we show by a digestion protection assay that OMVs are able to prevent enzymatic degradation of given full-length transcripts (SsrS, CsrC,10Sa, and rnpB). In summary, we show that OMV-associated RNA is clearly different in distinct culture conditions and that at least a fraction of the extracellular RNA is associated as a full-length transcripts with OMVs, indicating that some RNAs are protected by OMVs and thereby leaving open the possibility that those might be functionally active.« less

Authors:
 [1];  [1];  [2];  [1];  [3];  [1];  [4];  [4];  [1];  [5]
+ Show Author Affiliations
  1. Univ. of Luxembourg, Esch-sur-Alzette (Luxembourg)
  2. Univ. of Luxembourg, Esch-sur-Alzette (Luxembourg); Helmholtz-Centre for Environmental Research - UFZ, Halle (Germany); German Centre for Integrative Biodiversity Research (iDiv), Leipzig (Germany)
  3. Univ. de Strasbourg, Strasbourg (France)
  4. Pacific Northwest Research Institute, Seattle, WA (United States)
  5. Univ. of Luxembourg, Esch-sur-Alzette (Luxembourg); Centre Hospitalier de Luxembourg (Luxembourg)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1471073
Grant/Contract Number:  
AC05-76RL01830; CORE Junior/14/BM/8066232; CORE/15/BM/10404093; CORE/16/BM/11276306; Extracellular RNA Communication Consortium (U01HL126496)
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Malabirade, Antoine, Habier, Janine, Heintz-Buschart, Anna, May, Patrick, Godet, Julien, Halder, Rashi, Etheridge, Alton, Galas, David, Wilmes, Paul, and Fritz, Joëlle V. The RNA Complement of Outer Membrane Vesicles From Salmonella enterica Serovar Typhimurium Under Distinct Culture Conditions. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.02015.
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Malabirade, Antoine, Habier, Janine, Heintz-Buschart, Anna, May, Patrick, Godet, Julien, Halder, Rashi, Etheridge, Alton, Galas, David, Wilmes, Paul, & Fritz, Joëlle V. The RNA Complement of Outer Membrane Vesicles From Salmonella enterica Serovar Typhimurium Under Distinct Culture Conditions. United States. https://doi.org/10.3389/fmicb.2018.02015
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Malabirade, Antoine, Habier, Janine, Heintz-Buschart, Anna, May, Patrick, Godet, Julien, Halder, Rashi, Etheridge, Alton, Galas, David, Wilmes, Paul, and Fritz, Joëlle V. Thu . "The RNA Complement of Outer Membrane Vesicles From Salmonella enterica Serovar Typhimurium Under Distinct Culture Conditions". United States. https://doi.org/10.3389/fmicb.2018.02015. https://www.osti.gov/servlets/purl/1471073.
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@article{osti_1471073,
title = {The RNA Complement of Outer Membrane Vesicles From Salmonella enterica Serovar Typhimurium Under Distinct Culture Conditions},
author = {Malabirade, Antoine and Habier, Janine and Heintz-Buschart, Anna and May, Patrick and Godet, Julien and Halder, Rashi and Etheridge, Alton and Galas, David and Wilmes, Paul and Fritz, Joëlle V.},
abstractNote = {Here, bacterial outer membrane vesicles (OMVs), as well as OMV-associated small RNAs, have been demonstrated to play a role in host–pathogen interactions. The presence of larger RNA transcripts in OMVs has been less studied and their potential role in host–pathogen interactions remains largely unknown. Here we analyze RNA from OMVs secreted by Salmonella enterica serovar Typhimurium (S. Typhimurium) cultured under different conditions, which mimic host–pathogen interactions. S. Typhimurium was grown to exponential and stationary growth phases in minimal growth control medium (phosphate-carbon-nitrogen, PCN), as well as in acidic and phosphate-depleted PCN, comparable to the macrophage environment and inducing therefore the expression of Salmonella pathogenicity island 2 (SPI-2) genes. Moreover, Salmonella pathogenicity island 1 (SPI-1), which is required for virulence during the intestinal phase of infection, was induced by culturing S. Typhimurium to the stationary phase in Lysogeny Broth (LB). For each condition, we identified OMV-associated RNAs that are enriched in the extracellular environment relative to the intracellular space. All RNA classes could be observed, but a vast majority of rRNA was exported in all conditions in variable proportions with a notable decrease in LB SPI-1 inducing media. Several mRNAs and ncRNAs were specifically enriched in/on OMVs dependent on the growth conditions. Important to note is that some RNAs showed identical read coverage profiles intracellularly and extracellularly, whereas distinct coverage patterns were observed for other transcripts, suggesting a specific processing or degradation. Moreover, PCR experiments confirmed that distinct RNAs were present in or on OMVs as full-length transcripts (IsrB-1/2; IsrA; ffs; SsrS; CsrC; pSLT035; 10Sa; rnpB; STM0277; sseB; STM0972; STM2606), whereas others seemed to be rather present in a processed or degraded form. Finally, we show by a digestion protection assay that OMVs are able to prevent enzymatic degradation of given full-length transcripts (SsrS, CsrC,10Sa, and rnpB). In summary, we show that OMV-associated RNA is clearly different in distinct culture conditions and that at least a fraction of the extracellular RNA is associated as a full-length transcripts with OMVs, indicating that some RNAs are protected by OMVs and thereby leaving open the possibility that those might be functionally active.},
doi = {10.3389/fmicb.2018.02015},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {United States},
year = {Thu Aug 30 00:00:00 EDT 2018},
month = {Thu Aug 30 00:00:00 EDT 2018}
}
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https://doi.org/10.3389/fmicb.2018.02015
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Small RNAs in cell-to-cell communications during bacterial infection
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Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways
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Spheres of Hope, Packets of Doom: the Good and Bad of Outer Membrane Vesicles in Interspecies and Ecological Dynamics
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Deciphering the Interplay between Two Independent Functions of the Small RNA Regulator SgrS in Salmonella
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ssrA (tmRNA) Plays a Role in Salmonella enterica Serovar Typhimurium Pathogenesis
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Functional Advantages Conferred by Extracellular Prokaryotic Membrane Vesicles
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Secretable Small RNAs via Outer Membrane Vesicles in Periodontal Pathogens
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Small noncoding RNA GcvB is a novel regulator of acid resistance in Escherichia coli
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Systems analysis of multiple regulator perturbations allows discovery of virulence factors in Salmonella
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Diverse Secreted Effectors Are Required for Salmonella Persistence in a Mouse Infection Model
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Functional Advantages of Porphyromonas gingivalis Vesicles
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Coordinated Regulation of Virulence during Systemic Infection of Salmonella enterica Serovar Typhimurium
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GogB Is an Anti-Inflammatory Effector that Limits Tissue Damage during Salmonella Infection through Interaction with Human FBXO22 and Skp1
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A Novel Mechanism of Host-Pathogen Interaction through sRNA in Bacterial Outer Membrane Vesicles
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6S RNA is involved in acid resistance and invasion of epithelial cells in Salmonella enterica serovar Typhimurium
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Outer Membrane Vesicles (OMVs) of Gram-negative Bacteria: A Perspective Update
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Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum
journal, January 2014

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Obstacles and opportunities in the functional analysis of extracellular vesicle RNA - an ISEV position paper
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Dynamics of Salmonella small RNA expression in non-growing bacteria located inside eukaryotic cells
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Extinction, coextinction and colonization dynamics in plant-hummingbird networks under climate change
text, January 2022

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    Works referencing / citing this record:

    RNA-Sequencing Analyses of Small Bacterial RNAs and their Emergence as Virulence Factors in Host-Pathogen Interactions
    journal, February 2020

    • Diallo, Idrissa; Provost, Patrick
    • International Journal of Molecular Sciences, Vol. 21, Issue 5
    • DOI: 10.3390/ijms21051627
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