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Proteomics Reveals the Molecular Underpinnings of Stronger Learning and Memory in Eastern Compared to Western Bees.

ABSTRACT: The eastern (Apis cerana cerana, Acc) and western (Apis mellifera ligustica, Aml) honeybee are two major honeybee species. Surprisingly, little is known about the fundamental molecular neurobiology of brain suborgans of Acc and Aml. We characterized and compared the proteomes of mushroom bodies (MBs), antennal lobes (ALs) and optical lobes (OLs) in the brain of both species, and biologically validated the functions related to learning and memory. Acc and Aml have evolved similar proteome signatures in MBs and OLs to drive the domain-specific neural activities. In MBs of both species, commonly enriched and enhanced functional groups related to protein metabolism and Ca²⁺ transport relative to ALs and OLs, suggests that proteins and Ca²⁺ are vital for consolidating learning and memory via modulation of synaptic structure and signal transduction. Furthermore, in OLs of both species, the mainly enriched ribonucleoside metabolism suggests its vital role as second messenger in promoting phototransduction. Notably, in ALs of both species, distinct proteome settings have shaped to prime olfactory learning and memory. In ALs of Acc, this is supported by the enriched cytoskeleton organization to sustain olfactory signaling through modulation of plasticity in glomeruli and intracellular transport. In ALs of Aml, however, the enriched functional groups implicated in hydrogen ion transport are indicative of their importance in supporting olfactory processes by regulation of synaptic transmission. The biological confirmation of enhanced activities of protein metabolism and signal transduction in ALs and MBs of Acc relative to in Aml demonstrates that a stronger sense of olfactory learning and memory has evolved in Acc. The reported first in-depth proteome data of honeybee brain suborgans provide a novel insight into the molecular basis of neurobiology, and is potentially useful for further neurological studies in honeybees and other insects.

SUBMITTER: Meng L

PROVIDER: S-EPMC5795390 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Honeybee brain has distHoneybee brain has distinct anatomical and functional regions, knowledge on molecular underpinnings of sub-organ to achieve the distinct neural function and the difference between the eastern and western honeybees are still missing. Here, the proteomes of three sub-organs of eastern and western honeybee brains were compared. Mushroom bodies (MBs) and optical lobes (OLs) may by employed similar proteome architectures to drive their domain-specific neural activity in both bee species. In MBs, protein metabolism and Ca2+ transmembrane transport are the key role players in driving the learning and memory by modulating the synaptic structure and signal transduction to consolidate memory trace. In OLs, ribonucleoside metabolism and energy production play major roles to underpin visual system by maintaining G-protein cycle and membrane electrical charge potential. However, in antennal lobes (ALs), it has evolved distinct proteome settings to prime the olfactory learning and memory in two bee species. In ALs of Apis cerana cerana (Acc), actin cytoskeleton organization is key for plasticity of glomeruli and intracellular transport to sustain the olfactory signaling. Whereas, in ALs of Apis mellifera ligustica (Aml), hydrogen and hydrogen ion transport are vital to support olfactory process by supplying energy and maintaining molecule transport. Noticeably, in ALs of Acc, the exclusively enriched functional groups acting as second messenger and neurontransmitter of signal transduction, and the enhanced protein metabolism to regulate the plasticity of synaptic structure for formation of memory, suggest that Acc may have evolved a better sense of smell than that of Aml. Our first proteome data is helpful as starting point for further analysis of neural activity in brain sub-area of honeybee and other insects.inct anatomical and functional regions, knowledge on molecular underpinnings of sub-organ to achieve the distinct neural function and the difference between the eastern and western honeybees are still missing. Here, the proteomes of three sub-organs of eastern and western honeybee brains were compared. Mushroom bodies (MBs) and optical lobes (OLs) may by employed similar proteome architectures to drive their domain-specific neural activity in both bee species. In MBs, protein metabolism and Ca2+ transmembrane transport are the key role players in driving the learning and memory by modulating the synaptic structure and signal transduction to consolidate memory trace. In OLs, ribonucleoside metabolism and energy production play major roles to underpin visual system by maintaining G-protein cycle and membrane electrical charge potential. However, in antennal lobes (ALs), it has evolved distinct proteome settings to prime the olfactory learning and memory in two bee species. In ALs of Apis cerana cerana (Acc), actin cytoskeleton organization is key for plasticity of glomeruli and intracellular transport to sustain the olfactory signaling. Whereas, in ALs of Apis mellifera ligustica (Aml), hydrogen and hydrogen ion transport are vital to support olfactory process by supplying energy and maintaining molecule transport. Noticeably, in ALs of Acc, the exclusively enriched functional groups acting as second messenger and neurontransmitter of signal transduction, and the enhanced protein metabolism to regulate the plasticity of synaptic structure for formation of memory, suggest that Acc may have evolved a better sense of smell than that of Aml. Our first proteome data is helpful as starting point for further analysis of neural activity in brain sub-area of honeybee and other insects.

Project description:Most insecticides are insect neurotoxins. Evidence is emerging that sublethal doses of these neurotoxins are affecting the learning and memory of both wild and managed bee colonies, exacerbating the negative effects of pesticide exposure and reducing individual foraging efficiency.Variation in methodologies and interpretation of results across studies has precluded the quantitative evaluation of these impacts that is needed to make recommendations for policy change. It is not clear whether robust effects occur under acute exposure regimes (often argued to be more field-realistic than the chronic regimes upon which many studies are based), for field-realistic dosages, and for pesticides other than neonicotinoids.Here we use meta-analysis to examine the impact of pesticides on bee performance in proboscis extension-based learning assays, the paradigm most commonly used to assess learning and memory in bees. We draw together 104 (learning) and 167 (memory) estimated effect sizes across a diverse range of studies.We detected significant negative effects of pesticides on learning and memory (i) at field realistic dosages, (ii) under both chronic and acute application, and (iii) for both neonicotinoid and non-neonicotinoid pesticides groups.We also expose key gaps in the literature that include a critical lack of studies on non-Apis bees, on larval exposure (potentially one of the major exposure routes), and on performance in alternative learning paradigms. Policy implications. Procedures for the registration of new pesticides within EU member states now typically require assessment of risks to pollinators if potential target crops are attractive to bees. However, our results provide robust quantitative evidence for subtle, sublethal effects, the consequences of which are unlikely to be detected within small-scale prelicensing laboratory or field trials, but can be critical when pesticides are used at a landscape scale. Our findings highlight the need for long-term postlicensing environmental safety monitoring as a requirement within licensing policy for plant protection products.

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Proteomics Reveals the Molecular Underpinnings of Stronger Learning and Memory in Eastern Compared to Western Bees.

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