Abstract
Honey bee pollination is a key ecosystem service to nature and agriculture. However, biosafety research on genetically modified crops rarely considers effects on nurse bees from intact colonies, even though they receive and primarily process the largest amount of pollen. The objective of this study was to analyze the response of nurse bees and their gut bacteria to pollen from Bt maize expressing three different insecticidal Cry proteins (Cry1A.105, Cry2Ab2, and Cry3Bb1). Naturally Cry proteins are produced by bacteria (Bacillus thuringiensis). Colonies of Apis mellifera carnica were kept during anthesis in flight cages on field plots with the Bt maize, two different conventionally bred maize varieties, and without cages, 1-km outside of the experimental maize field to allow ad libitum foraging to mixed pollen sources. During their 10-days life span, the consumption of Bt maize pollen had no effect on their survival rate, body weight and rates of pollen digestion compared to the conventional maize varieties. As indicated by ELISA-quantification of Cry1A.105 and Cry3Bb1, more than 98% of the recombinant proteins were degraded. Bacterial population sizes in the gut were not affected by the genetic modification. Bt-maize, conventional varieties and mixed pollen sources selected for significantly different bacterial communities which were, however, composed of the same dominant members, including Proteobacteria in the midgut and Lactobacillus sp. and Bifidobacterium sp. in the hindgut. Surprisingly, Cry proteins from natural sources, most likely B. thuringiensis, were detected in bees with no exposure to Bt maize. The natural occurrence of Cry proteins and the lack of detectable effects on nurse bees and their gut bacteria give no indication for harmful effects of this Bt maize on nurse honey bees.
Highlights
During the last 15 years several regions of the world have explored the increasing introduction of transgenic crops into agriculture [1] and a significant proportion of them have been engineered to produce insecticidal proteins which are naturally synthesized by bacteria summarized under the species name Bacillus thuringiensis [2,3]
All of the identified Terminal restriction fragments (T-RFs) in this study showed their highest similarities (97–99%) to bacterial 16S rRNA gene DNA sequences previously found in bees [25] (Table S2)
The detection of Cry proteins from gut material of A. mellifera in this study clearly indicates the presence of B. thuringiensis as an inhabitant of the gut, even though, on a theoretical basis, it cannot be excluded that Cry proteins would be produced by other yet unknown bacteria
Summary
During the last 15 years several regions of the world have explored the increasing introduction of transgenic crops into agriculture [1] and a significant proportion of them have been engineered to produce insecticidal proteins which are naturally synthesized by bacteria summarized under the species name Bacillus thuringiensis [2,3] Members of this species are considered to inhabit soil but they are found in other environmental niches including phylloplane [4] and insects [5]. The safe use of stacked Bt maize in agriculture requires their environmental risk assessment, in which unintended adverse effects on non-target organisms expected to share the same ecosystem are analyzed Cry proteins develop their toxicity by forming pores in the gut epithelium of their target insects as a consequence of binding to specific receptors in the epithelial membrane [6]. Stacked events may require a specific risk assessment beyond an evaluation of their single transformation events [7,8]
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