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

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-?B. The centrality of NF-?B 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.

SUBMITTER: Nazzi F

PROVIDER: S-EPMC3375299 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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

Nazzi Francesco F Brown Sam P SP Annoscia Desiderato D Del Piccolo Fabio F Di Prisco Gennaro G Varricchio Paola P Della Vedova Giorgio G Cattonaro Federica F Caprio Emilio E Pennacchio Francesco F

PLoS pathogens 20120614 6

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 parasit ...[more]

PMID: 22719246

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Project description:The cumulative evidence that perinatal events have long-lasting ripple effects through the life of livestock animals should impact future nutritional and management recommendations at the farm level. The implications of fetal programming due to malnutrition, including neonatal survival and lower birth weights, have been characterized, particularly during early and mid-gestation, when placental and early fetal stages are being developed. The accelerated fetal growth during late pregnancy has been known for some time, while the impact of maternal stressors during this time on fetal development and by extent its postnatal repercussions on health and performance are still being defined. Maternal stressors during late pregnancy cannot only influence colostrogenesis but also compromise adequate intestinal development in the fetus, thus, that further limits the newborn's ability to absorb nutrients, bioactive compounds, and immunity (i.e., immunoglobulins, cytokines, and immune cells) from colostrum. These negative effects set the newborn calf to a challenging start in life by compromising passive immunity and intestinal maturation needed to establish a mature postnatal mucosal immune system while needing to digest and absorb nutrients in milk or milk replacer. Besides the dense-nutrient content and immunity in colostrum, it contains bioactive compounds such as growth factors, hormones, and cholesterol as well as molecular signals or instructions [e.g., microRNAs (miRNAs) and long non-coding RNAs (lncRNAs)] transferred from mother to offspring with the aim to influence postnatal gut maturation. The recent change in paradigm regarding prenatal materno-fetal microbiota inoculation and likely the presence of microbiota in the developing fetus intestine needs to be addressed in future research in ruminants. There still much to know on what prenatal or postnatal factors may predispose neonates to become susceptible to enteropathogens (e.g., enterotoxigenic Escherichia coli), causing diarrhea. From the host-side of this host-pathogen interaction, molecular data such as fecal RNA could, over time, help fill those gaps in knowledge. In addition, merging this novel fecal RNA approach with more established microbiome techniques can provide a more holistic picture of an enteropathogenesis and potentially uncover control points that can be addressed through management or nutrition at the farm level to minimize preweaning morbidity and mortality.

Dataset Information

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

Publications

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

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