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Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies.

Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P, Della Vedova G, Cattonaro F, Caprio E, Pennacchio F - PLoS Pathog. (2012)

Bottom Line: The de-stabilisation of DWV infection is associated with an immunosuppression syndrome, characterized by a strong down-regulation of the transcription factor NF-κB.The centrality of NF-κB in host responses to a range of environmental challenges suggests that this transcription factor can act as a common currency underlying colony collapse that may be triggered by different causes.Our results offer an integrated account for the multifactorial origin of honeybee losses and a new framework for assessing, and possibly mitigating, the impact of environmental challenges on honeybee health.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Udine, Udine, Italy. francesco.nazzi@uniud.it

ABSTRACT
The health of the honeybee and, indirectly, global crop production are threatened by several biotic and abiotic factors, which play a poorly defined role in the induction of widespread colony losses. Recent descriptive studies suggest that colony losses are often related to the interaction between pathogens and other stress factors, including parasites. Through an integrated analysis of the population and molecular changes associated with the collapse of honeybee colonies infested by the parasitic mite Varroa destructor, we show that this parasite can de-stabilise the within-host dynamics of Deformed wing virus (DWV), transforming a cryptic and vertically transmitted virus into a rapidly replicating killer, which attains lethal levels late in the season. The de-stabilisation of DWV infection is associated with an immunosuppression syndrome, characterized by a strong down-regulation of the transcription factor NF-κB. The centrality of NF-κB in host responses to a range of environmental challenges suggests that this transcription factor can act as a common currency underlying colony collapse that may be triggered by different causes. Our results offer an integrated account for the multifactorial origin of honeybee losses and a new framework for assessing, and possibly mitigating, the impact of environmental challenges on honeybee health.

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Related in: MedlinePlus

Dorsal expression in virus free and virus infected bees.Dorsal copies in virus free and virus infected honeybee larvae, either infested or not with one Varroa mite, 12 days after cell sealing; the error bars indicate the standard deviation. Average viral load in infected bee larvae, uninfested or infested by the Varroa mite, was 2.40E+10 and 3.22E+12, respectively. Dorsal expression was significantly reduced in virus infected bees compared to virus free bees, while Varroa infestation did not affect gene expression.
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ppat-1002735-g004: Dorsal expression in virus free and virus infected bees.Dorsal copies in virus free and virus infected honeybee larvae, either infested or not with one Varroa mite, 12 days after cell sealing; the error bars indicate the standard deviation. Average viral load in infected bee larvae, uninfested or infested by the Varroa mite, was 2.40E+10 and 3.22E+12, respectively. Dorsal expression was significantly reduced in virus infected bees compared to virus free bees, while Varroa infestation did not affect gene expression.

Mentions: To tentatively assess the respective contribution of Varroa mites and DWV in the induction of the observed immunosuppression, we measured the transcriptional level of dorsal-1A in bees, either infected or not by DWV, as affected by infestation of Varroa mites in vitro. No significant differences in the level of the dorsal-1A transcript were induced by mite feeding in lab reared bees that resulted DWV-free at the end of the experiment; conversely the expression level of dorsal-1A in lab reared bees infected by DWV was significantly lower than in the case of virus-free individuals, irrespective of their exposure to mite infestation (F = 26.79, df = 1: P<0.001; Figure 4). This result indirectly indicates that the virus may play an important role in the observed transcriptional down-regulation of dorsal-1A, which could be considered part of the virulence strategy adopted by DWV to overcome one of the central components of the antiviral immunity in insects [39]–[45].


Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies.

Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P, Della Vedova G, Cattonaro F, Caprio E, Pennacchio F - PLoS Pathog. (2012)

Dorsal expression in virus free and virus infected bees.Dorsal copies in virus free and virus infected honeybee larvae, either infested or not with one Varroa mite, 12 days after cell sealing; the error bars indicate the standard deviation. Average viral load in infected bee larvae, uninfested or infested by the Varroa mite, was 2.40E+10 and 3.22E+12, respectively. Dorsal expression was significantly reduced in virus infected bees compared to virus free bees, while Varroa infestation did not affect gene expression.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3375299&req=5

ppat-1002735-g004: Dorsal expression in virus free and virus infected bees.Dorsal copies in virus free and virus infected honeybee larvae, either infested or not with one Varroa mite, 12 days after cell sealing; the error bars indicate the standard deviation. Average viral load in infected bee larvae, uninfested or infested by the Varroa mite, was 2.40E+10 and 3.22E+12, respectively. Dorsal expression was significantly reduced in virus infected bees compared to virus free bees, while Varroa infestation did not affect gene expression.
Mentions: To tentatively assess the respective contribution of Varroa mites and DWV in the induction of the observed immunosuppression, we measured the transcriptional level of dorsal-1A in bees, either infected or not by DWV, as affected by infestation of Varroa mites in vitro. No significant differences in the level of the dorsal-1A transcript were induced by mite feeding in lab reared bees that resulted DWV-free at the end of the experiment; conversely the expression level of dorsal-1A in lab reared bees infected by DWV was significantly lower than in the case of virus-free individuals, irrespective of their exposure to mite infestation (F = 26.79, df = 1: P<0.001; Figure 4). This result indirectly indicates that the virus may play an important role in the observed transcriptional down-regulation of dorsal-1A, which could be considered part of the virulence strategy adopted by DWV to overcome one of the central components of the antiviral immunity in insects [39]–[45].

Bottom Line: The de-stabilisation of DWV infection is associated with an immunosuppression syndrome, characterized by a strong down-regulation of the transcription factor NF-κB.The centrality of NF-κB in host responses to a range of environmental challenges suggests that this transcription factor can act as a common currency underlying colony collapse that may be triggered by different causes.Our results offer an integrated account for the multifactorial origin of honeybee losses and a new framework for assessing, and possibly mitigating, the impact of environmental challenges on honeybee health.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Udine, Udine, Italy. francesco.nazzi@uniud.it

ABSTRACT
The health of the honeybee and, indirectly, global crop production are threatened by several biotic and abiotic factors, which play a poorly defined role in the induction of widespread colony losses. Recent descriptive studies suggest that colony losses are often related to the interaction between pathogens and other stress factors, including parasites. Through an integrated analysis of the population and molecular changes associated with the collapse of honeybee colonies infested by the parasitic mite Varroa destructor, we show that this parasite can de-stabilise the within-host dynamics of Deformed wing virus (DWV), transforming a cryptic and vertically transmitted virus into a rapidly replicating killer, which attains lethal levels late in the season. The de-stabilisation of DWV infection is associated with an immunosuppression syndrome, characterized by a strong down-regulation of the transcription factor NF-κB. The centrality of NF-κB in host responses to a range of environmental challenges suggests that this transcription factor can act as a common currency underlying colony collapse that may be triggered by different causes. Our results offer an integrated account for the multifactorial origin of honeybee losses and a new framework for assessing, and possibly mitigating, the impact of environmental challenges on honeybee health.

Show MeSH
Related in: MedlinePlus