Orsay Virus Infection of Caenorhabditis elegans Is Modulated by Zinc and Dependent on Lipids

Casorla-Perez, Luis Alberto; Guennoun, Ranya; Cubillas, Ciro; Peng, Bo; Kornfeld, Kerry; Wang, David

doi:10.1128/jvi.01211-22

Cited by 9 publications

(9 citation statements)

References 108 publications

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“…Of these, hyl-1 , pcyt-2.1 , psd-1 , scp-1 , and T26C12.1 were amongst the OrV-specific genes and hyl-1 and scp-1 , which were significantly upregulated at 18 and 22 hpi respectively, are predicted to be regulatory genes. A general trend towards downregulation was observed, as previously described (Casorla-Perez et al, 2022a). However, the biosynthesis of unsaturated fatty acids was one of the most significant categories enriched in the common genes (Fig.…”

Section: Resultssupporting

confidence: 86%

Story of an infection: viral dynamics and host responses in theCaenorhabditis elegans-Orsay virus pathosystem

Castiglioni,

Olmo-Uceda,

Villena-Giménez

et al. 2023

Preprint

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SUMMARYOrsay virus (OrV) is the only known natural virus affectingCaenorhabditis elegans, with minimal impact on the worm’s fitness due to its robust innate immune response. This study aimed to understand the interactions betweenC. elegansand OrV by tracking the infection’s progression during larval development. Four distinct stages of infection were identified based on viral load, with a peak in capsid- encoding RNA2 coinciding with the first signs of viral egression. Transcriptomic analysis revealed temporal changes in gene expression and functions induced by the infection. A specific set of up- regulated genes remained active throughout the infection, and genes correlated and anticorrelated with virus accumulation were identified. Responses to OrV mirrored reactions to other biotic stressors, distinguishing between virus-specific responses and broader immune responses. Additionally, mutants of early response genes and defense-related processes showed altered viral load progression, uncovering new players in the antiviral defense response.

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Section: Resultssupporting

confidence: 86%

Story of an infection: viral dynamics and host responses in theCaenorhabditis elegans-Orsay virus pathosystem

Castiglioni,

Olmo-Uceda,

Villena-Giménez

et al. 2023

Preprint

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“…In C. elegans' bacterial environments there is no distinction between food (nutrition) and biotic environment. This overlap is likely significant, given that the lipid content of the nematodes plays a crucial role in viral infections (44). Our experiments suggest that the resistance to virus infection is not caused by nutritional deficits because supplementation with bacteria that enable virus infection does not recover susceptibility to the virus.…”

Section: Discussionmentioning

confidence: 80%

Natural monobacterial environments modulate viral infection inCaenorhabditis elegans

González

Félix

2023

Preprint

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The microbes associated with an organism play a pivotal role in modulating their host susceptibility to viral infections. However, the influence of individual microbes on viral infections is not well understood. Here, we examined the impact of 67 naturally bacterial associates onCaenorhabditis eleganssusceptibility to Orsay virus. Our findings reveal that viral infection ofC. elegansis significantly influenced by monobacterial environments. The majority of tested natural bacterial environments reducedC. elegans viral infection while some increased susceptibility compared to anEscherichia colienvironmental reference. The reduction in viral infection is not caused by degradation of the virions or poor nutrition ofC. elegansby the bacteria. The reduction in viral infection does not require known antiviral responses, including RNA interference and transcriptional regulation downstream of the RIG-I homolog DRH-1. However, one bacterium,LelliottiaJUb276, reduced susceptibility but does not induce resistance to viral infection indrh-1mutants. Our research underscores the importance of considering the natural biotic environment in studies of viral infections and provides insights for future research on host-microbes-virus interactions and viral immunity.AUTHOR CONTRIBUTIONSConceptualization: RG, MAF; Formal analysis: RG; Investigation: RG; Resources: MAF; Data Curation: RG; Writing - Original Draft: RG, MAF; Writing - Review & Editing: RG, MAF; Visualization: RG; Supervision: MAF; Project administration: RG, MAF; Funding acquisition: RG, MAF.

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“…Supplementation of C . elegans with chemicals has been shown to restore viral susceptibility on resistant genotypes; mutants with disturbed lipid metabolism restore susceptibility to infection after being supplemented with certain lipids [ 48 ]. Some bacterial strains have been shown to possess immunomodulatory properties even after being heat-killed [ 49 ].…”

Section: Discussionmentioning

confidence: 99%

“…Our experiments suggest that the resistance to virus infection is not caused by nutritional deficits because supplementation with bacteria that enable virus infection does not recover susceptibility to the virus. Supplementation of C. elegans with chemicals has been shown to restore viral susceptibility on resistant genotypes; mutants with disturbed lipid metabolism restore susceptibility to infection after being supplemented with certain lipids [48]. Some bacterial strains have been shown to possess immunomodulatory properties even after being heat-killed [49].…”

Section: Discussionmentioning

confidence: 99%

Naturally-associated bacteria modulate Orsay virus infection of Caenorhabditis elegans

González,

Félix

2024

PLoS Pathog

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Microbes associated with an organism can significantly modulate its susceptibility to viral infections, but our understanding of the influence of individual microbes remains limited. The nematode Caenorhabditis elegans is a model organism that in nature inhabits environments rich in bacteria. Here, we examine the impact of 71 naturally associated bacteria on C. elegans susceptibility to its only known natural virus, the Orsay virus. Our findings reveal that viral infection of C. elegans is significantly influenced by monobacterial environments. Compared to an Escherichia coli environmental reference, the majority of tested bacteria reduced C. elegans susceptibility to viral infection. This reduction is not caused by virion degradation or poor animal nutrition by the bacteria. The repression of viral infection by the bacterial strains Chryseobacterium JUb44 and Sphingobacterium BIGb0172 does not require the RIG-I homolog DRH-1, which is known to activate antiviral responses such as RNA interference and transcriptional regulation. Our research highlights the necessity of considering natural biotic environments in viral infection studies and opens the way future research on host-microbe-virus interactions.

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Orsay Virus Infection of Caenorhabditis elegans Is Modulated by Zinc and Dependent on Lipids

Abstract: Orsay virus is the only known natural virus pathogen of Caenorhabditis elegans , which shares many evolutionarily conserved pathways with humans. We leveraged the powerful genetic tractability of C. elegans to characterize a novel interaction between zinc, lipids, and virus infection.

Cited by 9 publications

References 108 publications

Story of an infection: viral dynamics and host responses in theCaenorhabditis elegans-Orsay virus pathosystem

Story of an infection: viral dynamics and host responses in theCaenorhabditis elegans-Orsay virus pathosystem

Natural monobacterial environments modulate viral infection inCaenorhabditis elegans

Naturally-associated bacteria modulate Orsay virus infection of Caenorhabditis elegans

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