Competitive fitness in coronaviruses is not correlated with size or number of double-membrane vesicles under reduced-temperature growth conditions.
Identifieur interne : 001687 ( Main/Exploration ); précédent : 001686; suivant : 001688Competitive fitness in coronaviruses is not correlated with size or number of double-membrane vesicles under reduced-temperature growth conditions.
Auteurs : Hawaa M N. Al-Mulla ; Lauren Turrell ; Nicola M. Smith ; Luke Payne ; Surendranath Baliji ; Roland Züst ; Volker Thiel ; Susan C. Baker ; Stuart G. Siddell ; Benjamin W. NeumanSource :
- mBio [ 2150-7511 ] ; 2014.
Descripteurs français
- KwdFr :
- Animaux, Cellules cultivées, Interactions hôte-pathogène, Microscopie électronique, Mutation, Protéines virales non structurales (génétique), Protéines virales non structurales (métabolisme), Réplication virale, Souris, Température, Virus de l'hépatite murine (croissance et développement), Virus de l'hépatite murine (physiologie), Vésicules cytoplasmiques (virologie).
- MESH :
- croissance et développement : Virus de l'hépatite murine.
- génétique : Protéines virales non structurales.
- métabolisme : Protéines virales non structurales.
- physiologie : Virus de l'hépatite murine.
- virologie : Vésicules cytoplasmiques.
- Animaux, Cellules cultivées, Interactions hôte-pathogène, Microscopie électronique, Mutation, Réplication virale, Souris, Température.
English descriptors
- KwdEn :
- Animals, Cells, Cultured, Cytoplasmic Vesicles (virology), Host-Pathogen Interactions, Mice, Microscopy, Electron, Murine hepatitis virus (growth & development), Murine hepatitis virus (physiology), Mutation, Temperature, Viral Nonstructural Proteins (genetics), Viral Nonstructural Proteins (metabolism), Virus Replication.
- MESH :
- chemical , genetics : Viral Nonstructural Proteins.
- growth & development : Murine hepatitis virus.
- chemical , metabolism : Viral Nonstructural Proteins.
- physiology : Murine hepatitis virus.
- virology : Cytoplasmic Vesicles.
- Animals, Cells, Cultured, Host-Pathogen Interactions, Mice, Microscopy, Electron, Mutation, Temperature, Virus Replication.
Abstract
Positive-stranded viruses synthesize their RNA in membrane-bound organelles, but it is not clear how this benefits the virus or the host. For coronaviruses, these organelles take the form of double-membrane vesicles (DMVs) interconnected by a convoluted membrane network. We used electron microscopy to identify murine coronaviruses with mutations in nsp3 and nsp14 that replicated normally while producing only half the normal amount of DMVs under low-temperature growth conditions. Viruses with mutations in nsp5 and nsp16 produced small DMVs but also replicated normally. Quantitative reverse transcriptase PCR (RT-PCR) confirmed that the most strongly affected of these, the nsp3 mutant, produced more viral RNA than wild-type virus. Competitive growth assays were carried out in both continuous and primary cells to better understand the contribution of DMVs to viral fitness. Surprisingly, several viruses that produced fewer or smaller DMVs showed a higher fitness than wild-type virus at the reduced temperature, suggesting that larger and more numerous DMVs do not necessarily confer a competitive advantage in primary or continuous cell culture. For the first time, this directly demonstrates that replication and organelle formation may be, at least in part, studied separately during infection with positive-stranded RNA virus. IMPORTANCE The viruses that cause severe acute respiratory syndrome (SARS), poliomyelitis, and hepatitis C all replicate in double-membrane vesicles (DMVs). The big question about DMVs is why they exist in the first place. In this study, we looked at thousands of infected cells and identified two coronavirus mutants that made half as many organelles as normal and two others that made typical numbers but smaller organelles. Despite differences in DMV size and number, all four mutants replicated as efficiently as wild-type virus. To better understand the relative importance of replicative organelles, we carried out competitive fitness experiments. None of these viruses was found to be significantly less fit than wild-type, and two were actually fitter in tests in two kinds of cells. This suggests that viruses have evolved to have tremendous plasticity in the ability to form membrane-associated replication complexes and that large and numerous DMVs are not exclusively associated with efficient coronavirus replication.
DOI: 10.1128/mBio.01107-13
PubMed: 24692638
Affiliations:
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Le document en format XML
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<term>Mice</term>
<term>Microscopy, Electron</term>
<term>Murine hepatitis virus (growth & development)</term>
<term>Murine hepatitis virus (physiology)</term>
<term>Mutation</term>
<term>Temperature</term>
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<term>Viral Nonstructural Proteins (metabolism)</term>
<term>Virus Replication</term>
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<term>Protéines virales non structurales (métabolisme)</term>
<term>Réplication virale</term>
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<front><div type="abstract" xml:lang="en">Positive-stranded viruses synthesize their RNA in membrane-bound organelles, but it is not clear how this benefits the virus or the host. For coronaviruses, these organelles take the form of double-membrane vesicles (DMVs) interconnected by a convoluted membrane network. We used electron microscopy to identify murine coronaviruses with mutations in nsp3 and nsp14 that replicated normally while producing only half the normal amount of DMVs under low-temperature growth conditions. Viruses with mutations in nsp5 and nsp16 produced small DMVs but also replicated normally. Quantitative reverse transcriptase PCR (RT-PCR) confirmed that the most strongly affected of these, the nsp3 mutant, produced more viral RNA than wild-type virus. Competitive growth assays were carried out in both continuous and primary cells to better understand the contribution of DMVs to viral fitness. Surprisingly, several viruses that produced fewer or smaller DMVs showed a higher fitness than wild-type virus at the reduced temperature, suggesting that larger and more numerous DMVs do not necessarily confer a competitive advantage in primary or continuous cell culture. For the first time, this directly demonstrates that replication and organelle formation may be, at least in part, studied separately during infection with positive-stranded RNA virus. IMPORTANCE The viruses that cause severe acute respiratory syndrome (SARS), poliomyelitis, and hepatitis C all replicate in double-membrane vesicles (DMVs). The big question about DMVs is why they exist in the first place. In this study, we looked at thousands of infected cells and identified two coronavirus mutants that made half as many organelles as normal and two others that made typical numbers but smaller organelles. Despite differences in DMV size and number, all four mutants replicated as efficiently as wild-type virus. To better understand the relative importance of replicative organelles, we carried out competitive fitness experiments. None of these viruses was found to be significantly less fit than wild-type, and two were actually fitter in tests in two kinds of cells. This suggests that viruses have evolved to have tremendous plasticity in the ability to form membrane-associated replication complexes and that large and numerous DMVs are not exclusively associated with efficient coronavirus replication.</div>
</front>
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<tree><noCountry><name sortKey="Al Mulla, Hawaa M N" sort="Al Mulla, Hawaa M N" uniqKey="Al Mulla H" first="Hawaa M N" last="Al-Mulla">Hawaa M N. Al-Mulla</name>
<name sortKey="Baker, Susan C" sort="Baker, Susan C" uniqKey="Baker S" first="Susan C" last="Baker">Susan C. Baker</name>
<name sortKey="Baliji, Surendranath" sort="Baliji, Surendranath" uniqKey="Baliji S" first="Surendranath" last="Baliji">Surendranath Baliji</name>
<name sortKey="Neuman, Benjamin W" sort="Neuman, Benjamin W" uniqKey="Neuman B" first="Benjamin W" last="Neuman">Benjamin W. Neuman</name>
<name sortKey="Payne, Luke" sort="Payne, Luke" uniqKey="Payne L" first="Luke" last="Payne">Luke Payne</name>
<name sortKey="Siddell, Stuart G" sort="Siddell, Stuart G" uniqKey="Siddell S" first="Stuart G" last="Siddell">Stuart G. Siddell</name>
<name sortKey="Smith, Nicola M" sort="Smith, Nicola M" uniqKey="Smith N" first="Nicola M" last="Smith">Nicola M. Smith</name>
<name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name>
<name sortKey="Turrell, Lauren" sort="Turrell, Lauren" uniqKey="Turrell L" first="Lauren" last="Turrell">Lauren Turrell</name>
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