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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

Seasonal dynamics of bees in colonies with low and high levels of mite infestation.(A) Estimated bee numbers recorded in each hive in October, when a sudden decrease of bee population was observed in highly infested colonies. (B) Bee mortality over time. The error bars indicate the standard deviation; mean values significantly different are denoted with asterisks (*P≤0.05; **P≤0.01). Bee population in highly infested colonies reached minimum levels in October, because of a marked increase of bee mortality.
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ppat-1002735-g001: Seasonal dynamics of bees in colonies with low and high levels of mite infestation.(A) Estimated bee numbers recorded in each hive in October, when a sudden decrease of bee population was observed in highly infested colonies. (B) Bee mortality over time. The error bars indicate the standard deviation; mean values significantly different are denoted with asterisks (*P≤0.05; **P≤0.01). Bee population in highly infested colonies reached minimum levels in October, because of a marked increase of bee mortality.

Mentions: A decline of bee population was observed in all colonies along the Summer, although a marked acceleration of the process was noted in HIC late in the season so that, at the end of October, a significant reduction of bee population was observed in such colonies (U = 0, n1 = 6, n2 = 5: P<0.01; Figure 1A). Two highly infested colonies collapsed by the end of Autumn, whereas the remaining ones did so by the following Spring. Bee mortality, as determined from the number of dead bees recovered in front of the hives and bee population, was abruptly and significantly raised at the end of the season in HIC (U = 0, n1 = 6, n2 = 5: P<0.01; Figure 1B).


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)

Seasonal dynamics of bees in colonies with low and high levels of mite infestation.(A) Estimated bee numbers recorded in each hive in October, when a sudden decrease of bee population was observed in highly infested colonies. (B) Bee mortality over time. The error bars indicate the standard deviation; mean values significantly different are denoted with asterisks (*P≤0.05; **P≤0.01). Bee population in highly infested colonies reached minimum levels in October, because of a marked increase of bee mortality.
© Copyright Policy
Related In: Results  -  Collection

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

ppat-1002735-g001: Seasonal dynamics of bees in colonies with low and high levels of mite infestation.(A) Estimated bee numbers recorded in each hive in October, when a sudden decrease of bee population was observed in highly infested colonies. (B) Bee mortality over time. The error bars indicate the standard deviation; mean values significantly different are denoted with asterisks (*P≤0.05; **P≤0.01). Bee population in highly infested colonies reached minimum levels in October, because of a marked increase of bee mortality.
Mentions: A decline of bee population was observed in all colonies along the Summer, although a marked acceleration of the process was noted in HIC late in the season so that, at the end of October, a significant reduction of bee population was observed in such colonies (U = 0, n1 = 6, n2 = 5: P<0.01; Figure 1A). Two highly infested colonies collapsed by the end of Autumn, whereas the remaining ones did so by the following Spring. Bee mortality, as determined from the number of dead bees recovered in front of the hives and bee population, was abruptly and significantly raised at the end of the season in HIC (U = 0, n1 = 6, n2 = 5: P<0.01; Figure 1B).

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