Increase in Gut Microbiota After Immune Suppression in Baculovirus-infected Larvae

Overview

Journal PLoS Pathog

Specialty Microbiology

Date 2013 May 30

PMID 23717206

Citations 30

Authors

Agata K Jakubowska

Heiko Vogel

Salvador Herrero

Affiliations

Soon will be listed here.

Abstract

Spodoptera exigua microarray was used to determine genes differentially expressed in S. exigua cells challenged with the species-specific baculovirus SeMNPV as well as with a generalist baculovirus, AcMNPV. Microarray results revealed that, in contrast to the host transcriptional shut-off that is expected during baculovirus infection, S. exigua cells showed a balanced number of up- and down-regulated genes during the first 36 hours following the infection. Many immune-related genes, including pattern recognition proteins, genes involved in signalling and immune pathways as well as immune effectors and genes coding for proteins involved in the melanization cascade were found to be down-regulated after baculovirus infection. The down-regulation of immune-related genes was confirmed in the larval gut. The expression of immune-related genes in the gut is known to affect the status of gut microorganisms, many of which are responsible for growth and development functions. We therefore asked whether the down-regulation that occurs after baculovirus infection affects the amount of gut microbiota. An increase in the gut bacterial load was observed and we hypothesize this to be as a consequence of viral infection. Subsequent experiments on virus performance in the presence and absence of gut microbiota revealed that gut bacteria enhanced baculovirus virulence, pathogenicity and dispersion. We discuss the host immune response processes and pathways affected by baculoviruses, as well as the role of gut microbiota in viral infection.

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References

Qin X, Singh K, Weinstock G, Murray B . Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J Bacteriol. 2001; 183(11):3372-82. PMC: 99635. DOI: 10.1128/JB.183.11.3372-3382.2001. View

Kingsolver M, Hardy R . Making connections in insect innate immunity. Proc Natl Acad Sci U S A. 2012; 109(46):18639-40. PMC: 3503154. DOI: 10.1073/pnas.1216736109. View

Wilks J, Golovkina T . Influence of microbiota on viral infections. PLoS Pathog. 2012; 8(5):e1002681. PMC: 3355081. DOI: 10.1371/journal.ppat.1002681. View

Hirai M, Terenius O, Li W, Faye I . Baculovirus and dsRNA induce Hemolin, but no antibacterial activity, in Antheraea pernyi. Insect Mol Biol. 2004; 13(4):399-405. DOI: 10.1111/j.0962-1075.2004.00497.x. View

Popham H, Grasela J, Goodman C, McIntosh A . Baculovirus infection influences host protein expression in two established insect cell lines. J Insect Physiol. 2010; 56(9):1237-45. DOI: 10.1016/j.jinsphys.2010.03.024. View

Jarosz J . Gut flora of Galleria mellonella suppressing ingested bacteria. J Invertebr Pathol. 1979; 34(2):192-8. DOI: 10.1016/0022-2011(79)90101-0. View

Nobiron I, OReilly D, Olszewski J . Autographa californica nucleopolyhedrovirus infection of Spodoptera frugiperda cells: a global analysis of host gene regulation during infection, using a differential display approach. J Gen Virol. 2003; 84(Pt 11):3029-3039. DOI: 10.1099/vir.0.19270-0. View

Jayachandran B, Hussain M, Asgari S . RNA interference as a cellular defense mechanism against the DNA virus baculovirus. J Virol. 2012; 86(24):13729-34. PMC: 3503065. DOI: 10.1128/JVI.02041-12. View

Raymond B, Vanbergen A, Pearce I, Hartley S, Cory J, Hails R . Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus. Oecologia. 2017; 131(4):533-541. DOI: 10.1007/s00442-002-0926-4. View

10.

Kounatidis I, Ligoxygakis P . Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biol. 2012; 2(5):120075. PMC: 3376734. DOI: 10.1098/rsob.120075. View

11.

Cerf-Bensussan N, Gaboriau-Routhiau V . The immune system and the gut microbiota: friends or foes?. Nat Rev Immunol. 2010; 10(10):735-44. DOI: 10.1038/nri2850. View

12.

Ponton F, Chapuis M, Pernice M, Sword G, Simpson S . Evaluation of potential reference genes for reverse transcription-qPCR studies of physiological responses in Drosophila melanogaster. J Insect Physiol. 2011; 57(6):840-50. DOI: 10.1016/j.jinsphys.2011.03.014. View

13.

Lemaitre B, Hoffmann J . The host defense of Drosophila melanogaster. Annu Rev Immunol. 2007; 25:697-743. DOI: 10.1146/annurev.immunol.25.022106.141615. View

14.

Hernandez-Martinez P, Naseri B, Navarro-Cerrillo G, Escriche B, Ferre J, Herrero S . Increase in midgut microbiota load induces an apparent immune priming and increases tolerance to Bacillus thuringiensis. Environ Microbiol. 2010; 12(10):2730-7. DOI: 10.1111/j.1462-2920.2010.02241.x. View

15.

Breitenbach J, Shelby K, Popham H . Baculovirus induced transcripts in hemocytes from the larvae of Heliothis virescens. Viruses. 2011; 3(11):2047-64. PMC: 3230841. DOI: 10.3390/v3112047. View

16.

Trudeau D, Washburn J, Volkman L . Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. J Virol. 2001; 75(2):996-1003. PMC: 113996. DOI: 10.1128/JVI.75.2.996-1003.2001. View

17.

Ooi B, Miller L . Regulation of host RNA levels during baculovirus infection. Virology. 1988; 166(2):515-23. DOI: 10.1016/0042-6822(88)90522-3. View

18.

Munoz D, Murillo R, Krell P, Vlak J, Caballero P . Four genotypic variants of a Spodoptera exigua Nucleopolyhedrovirus (Se-SP2) are distinguishable by a hypervariable genomic region. Virus Res. 2000; 59(1):61-74. DOI: 10.1016/s0168-1702(98)00125-7. View

19.

Kane M, Case L, Kopaskie K, Kozlova A, MacDearmid C, Chervonsky A . Successful transmission of a retrovirus depends on the commensal microbiota. Science. 2011; 334(6053):245-9. PMC: 3519937. DOI: 10.1126/science.1210718. View

20.

Singh J, Singh C, Bhavani A, Nagaraju J . Discovering microRNAs from Bombyx mori nucleopolyhedrosis virus. Virology. 2010; 407(1):120-8. DOI: 10.1016/j.virol.2010.07.033. View