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Open AccessArticle

Characterization of Venom Components and Their Phylogenetic Properties in Some Aculeate Bumblebees and Wasps

1
Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea
2
Department of Agricultural Biology, Seoul National University, Seoul 08826, Korea
3
EntoCode Co., Seoul 06028, Korea
4
National Institute of Biological Resources, Environmental Research Complex, Incheon 22689, Korea
*
Authors to whom correspondence should be addressed.
Toxins 2020, 12(1), 47; https://doi.org/10.3390/toxins12010047 (registering DOI)
Received: 14 December 2019 / Revised: 9 January 2020 / Accepted: 11 January 2020 / Published: 14 January 2020
(This article belongs to the Special Issue Evolutionary Ecology of Venom)
To identify and compare venom components and expression patterns, venom gland-specific transcriptome analyses were conducted for 14 Aculeate bees and wasps. TPM (transcripts per kilobase million) values were normalized using the average transcription level of a reference housekeeping gene (dimethyladenosine transferase). Orthologous venom component genes across the 14 bee and wasp species were identified, and their relative abundance in each species was determined by comparing normalized TPM values. Based on signal sequences in the transcripts, the genes of novel venom components were identified and characterized to encode potential allergens. Most of the allergens and pain-producing factors (arginine kinase, hyaluronidase, mastoparan, phospholipase A1, phospholipase A2, and venom allergen 5) showed extremely high expression levels in social wasps. Acid phosphatase, neprilysin, and tachykinin, which are known allergens and neurotoxic peptides, were found in the venom glands of solitary wasps more often than in social wasps. In the venom glands of bumblebees, few or no transcripts of major allergens or pain-producing factors were identified. Taken together, these results indicate that differential expression patterns of the venom genes in some Aculeate species imply that some wasps and bumblebee species have unique groups of highly expressed venom components. Some venom components reflected the Aculeate species phylogeny, but others did not. This unique evolution of specific venom components in different groups of some wasps and bumblebee species might have been shaped in response to both ecological and behavioral influences. View Full-Text
Keywords: venom; social wasp; solitary hunting wasp; bumblebee; venom gland; transcriptome analysis venom; social wasp; solitary hunting wasp; bumblebee; venom gland; transcriptome analysis
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Yoon, K.A.; Kim, K.; Kim, W.-J.; Bang, W.Y.; Ahn, N.-H.; Bae, C.-H.; Yeo, J.-H.; Lee, S.H. Characterization of Venom Components and Their Phylogenetic Properties in Some Aculeate Bumblebees and Wasps. Toxins 2020, 12, 47.

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    Doi: 10.5281/zenodo.3605769
    Link: http://zenodo.org/record/3605769
    Description: The following are available online at www.mdpi.com/xxx/s1, Figure S1: Comparison of the relative transcription levels and TPM values of A) arginine kinase, B) defensin 1, C) dipeptidyl peptidase 4, D) hyaluronidase, E) icarapin, F) phospholipase A2, G) serine protease inhibitor, H) tachykinin, I) vitallogenin and J) neprilysin from P. rothneyi, P. snelleni, E. decoratus and B. ardens, Figure S2: Amino acid alignments of uncharacterized protein 1 from V. crabro, V. simillima, P. varia, P. snelleni, B. consobrinus and M. banksi, Figure S3: Amino acid alignments of uncharacterized protein 2 from V. analis, V. dybowskii, P. varia, A. flavomarginatum and Crassostrea gigas, Figure S4: Amino acid alignments of uncharacterized protein 3 from V. dybowskii, B. consobrinus, B. ussurensis and Hevea brasiliensis, Figure S5: Amino acid alignments of uncharacterized protein 4 from B. ardens, B. ussurensis and Triticum aestivum, Figure S6: Amino acid alignments of uncharacterized protein 5 from P. varia, A. flavomarginatum and S. geminate, Figure S7: Amino acid alignments of uncharacterized protein 6 from V. dybowskii and A. flavomarginatum, Figure S8: Amino acid alignments of carboxylesterase 6. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, Sphecidae sp., B. ussurensis and S. mimosarum. B) Phylogenetic analysis of carboxylesterase 6, Figure S9: Amino acid alignments of dipeptidyl peptidase 4. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. rothneyi, A. flavomarginatum, S. deforme, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and P. tepidariorum. B) Phylogenetic analysis of dipeptidyl peptidase 4, Figure S10: Amino acid alignments of endocuticle structural glycoprotein. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, B. consobrinus, B. ussurensis and Blattella germanica. B) Phylogenetic analysis of endocuticle structural glycoprotein, Figure S11: Amino acid alignments of icarapin. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and O. monticola. B) Phylogenetic analysis of icarapin, Figure S12: Amino acid alignments of major royal jelly protein. A) Alignment of amino acid sequences from P. varia, P. rothneyi, E. decoratus, S. deforme, B. ardens, B. consobrinus, B. ussurensis and P. tepidariorum. B) Phylogenetic analysis of major royal jelly protein, Figure S13: Amino acid alignments of phospholipase B. A) Alignment of amino acid sequences from V. analis, P. varia, P. snelleni, P. rothneyi, E. decoratus, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and H. spadix. B) Phylogenetic analysis of phospholipase B, Figure S14: Amino acid alignments of serine protease inhibitor. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. consobrinus and B. germanica. B) Phylogenetic analysis of serine protease inhibitor, Figure S15: Amino acid alignments of vitellogenin. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and B. germanica. B) Phylogenetic analysis of vitellogenin, Figure S16: Amino acid alignments of acid phosphatase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, P. varia, P. snelleni, A. flavomarginatum, S. deforme, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and H. sapiens. B) Phylogenetic analysis of acid phosphatase, Figure S17: Amino acid alignments of defensin 2. A) Alignment of amino acid sequences from P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, Sphecidae sp. and H. sapiens. B) Phylogenetic analysis of defensin 2, Figure S18: Amino acid alignments of hyaluronidase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, S. deforme, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of hyaluronidase, Figure S19: Amino acid alignments of mastoparan. A) Alignment of amino acid sequences from V. crabro, V. analis, P. snelleni, P. rothneyi, A. flavomarginatum, S. deforme, B. ussurensis and uncultured bacterium. B) Phylogenetic analysis of mastoparan, Figure S20: Amino acid alignments of metalloproteinase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of metalloproteinase, Figure S21: Amino acid alignments of neprilysin. A) Alignment of amino acid sequences from A. flavomarginatum, E. decoratus, B. consobrinus and B. germanica. B) Phylogenetic analysis of neprilysin, Figure S22: Amino acid alignments of phospholipase A1. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. rothneyi, E. decoratus, B. consobrinus, B. ussurensis and H. spadix. B) Phylogenetic analysis of phospholipase A1, Figure S23: Amino acid alignments of serine carboxypeptidase. A) Alignment of amino acid sequences from V. crabro, V. analis, P. varia, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. consobrinus and B. germanica. B) Phylogenetic analysis of serine carboxypeptidase, Figure S24: Amino acid alignments of serine protease. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decorates, S. deforme, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of serine protease, Figure S1: Amino acid alignments of acid phosphatase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, P. varia, P. snelleni, A. flavomarginatum, S. deforme, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and H. sapiens. B) Phylogenetic analysis of acid phosphatase., Figure S25: Amino acid alignments of arginine kinase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. consobrinus and Hadrurus spadix. B) Phylogenetic analysis of arginine kinase, Figure S3: Amino acid alignments of carboxylesterase 6. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, Sphecidae sp., B. ussurensis and S. mimosarum. B) Phylogenetic analysis of carboxylesterase 6, Figure S426: Amino acid alignments of defensin 1. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, P. varia, P. rothneyi, A. flavomarginatum, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and H. sapiens. B) Phylogenetic analysis of defensin 1, Figure S5: Amino acid alignments of defensin 2. A) Alignment of amino acid sequences from P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, Sphecidae sp. and H. sapiens. B) Phylogenetic analysis of defensin 2, Figure S6: Amino acid alignments of dipeptidyl peptidase 4. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. rothneyi, A. flavomarginatum, S. deforme, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and P. tepidariorum. B) Phylogenetic analysis of dipeptidyl peptidase 4, Figure S7: Amino acid alignments of endocuticle structural glycoprotein. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, B. consobrinus, B. ussurensis and Blattella germanica. B) Phylogenetic analysis of endocuticle structural glycoprotein, Figure S8: Amino acid alignments of hyaluronidase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, S. deforme, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of hyaluronidase, Figure S9: Amino acid alignments of icarapin. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and O. monticola. B) Phylogenetic analysis of icarapin, Figure S10: Amino acid alignments of major royal jelly protein. A) Alignment of amino acid sequences from P. varia, P. rothneyi, E. decoratus, S. deforme, B. ardens, B. consobrinus, B. ussurensis and P. tepidariorum. B) Phylogenetic analysis of major royal jelly protein, Figure S11: Amino acid alignments of mastoparan. A) Alignment of amino acid sequences from V. crabro, V. analis, P. snelleni, P. rothneyi, A. flavomarginatum, S. deforme, B. ussurensis and uncultured bacterium. B) Phylogenetic analysis of mastoparan, Figure S12: Amino acid alignments of metalloproteinase. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of metalloproteinase, Figure S13: Amino acid alignments of neprilysin. A) Alignment of amino acid sequences from A. flavomarginatum, E. decoratus, B. consobrinus and B. germanica. B) Phylogenetic analysis of neprilysin, Figure S14: Amino acid alignments of phospholipase A1. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. rothneyi, E. decoratus, B. consobrinus, B. ussurensis and H. spadix. B) Phylogenetic analysis of phospholipase A1, Figure S1527: Amino acid alignments of phospholipase A2. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. rothneyi, A. flavomarginatum, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of phospholipase A2, Figure S16: Amino acid alignments of phospholipase B. A) Alignment of amino acid sequences from V. analis, P. varia, P. snelleni, P. rothneyi, E. decoratus, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and H. spadix. B) Phylogenetic analysis of phospholipase B, Figure S17: Amino acid alignments of serine carboxypeptidase. A) Alignment of amino acid sequences from V. crabro, V. analis, P. varia, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. consobrinus and B. germanica. B) Phylogenetic analysis of serine carboxypeptidase, Figure S18: Amino acid alignments of serine protease. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decorates, S. deforme, Sphecidae sp., B. ardens, B. ussurensis and H. sapiens. B) Phylogenetic analysis of serine protease, Figure S19: Amino acid alignments of serine protease inhibitor. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, E. decoratus, S. deforme, Sphecidae sp., B. ardens, B. consobrinus and B. germanica. B) Phylogenetic analysis of serine protease inhibitor, Figure S208: Amino acid alignments of tachykinin. A) Alignment of amino acid sequences from V. analis, V. dybowskii, P. varia, P. snelleni, P. rothneyi, E. decorates, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis, and B. germanica. B) Phylogenetic analysis of tachykinin, Figure S219: Amino acid alignments of venom allergen 5. A) Alignment of amino acid sequences from V. crabro, V. analis, V. simillima, P. snelleni, P. rothneyi, A. flavomarginatum, S. deforme, Sphecidae sp., B. ussurensis and Varroa destructor. B) Phylogenetic analysis of venom allergen 5, Figure S22: Amino acid alignments of vitellogenin. A) Alignment of amino acid sequences from V. crabro, V. analis, V. dybowskii, V. simillima, P. varia, P. snelleni, P. rothneyi, A. flavomarginatum, Sphecidae sp., B. ardens, B. consobrinus, B. ussurensis and B. germanica. B) Phylogenetic analysis of vitellogenin, Figure S23: Amino acid alignments of uncharacterized protein 1 from V. crabro, V. simillima, P. varia, P. snelleni, B. consobrinus and M. banksi, Figure S24: Amino acid alignments of uncharacterized protein 2 from V. analis, V. dybowskii, P. varia, A. flavomarginatum and Crassostrea gigas, Figure S25: Amino acid alignments of uncharacterized protein 3 from V. dybowskii, B. consobrinus, B. ussurensis and Hevea brasiliensis, Figure S26: Amino acid alignments of uncharacterized protein 4 from B. ardens, B. ussurensis and Triticum aestivum, Figure S27: Amino acid alignments of uncharacterized protein 5 from P. varia, A. flavomarginatum and S. geminate, Figure S28: Amino acid alignments of uncharacterized protein 6 from V. dybowskii and A. flavomarginatum, Figure S29: Comparison of the relative transcription levels and TPM values of A) arginine kinase, B) defensin 1, C) dipeptidyl peptidase 4, D) hyaluronidase, E) icarapin, F) phospholipase A2, G) serine protease inhibitor, H) tachykinin, I) vitallogenin and J) neprilysin from P. rothneyi, P. snelleni, E. decoratus and B. ardens. Table S1: Annotation of top 100 highly expressed genes in the venom gland of Vespa analistable caption, Table S2: Annotation of top 100 highly expressed genes in the venom gland of Vespa crabrotable caption, Table S3: Annotation of top 100 highly expressed genes in the venom gland of Vespa dybowskiitable caption, Table S4: Annotation of top 100 highly expressed genes in the venom gland of Vespa simillimatable caption, Table S5: Annotation of top 100 highly expressed genes in the venom gland of Parapolybia variatable caption, Table S6: Annotation of top 100 highly expressed genes in the venom gland of Polistes rothneyitable caption, Table S7: Annotation of top 100 highly expressed genes in the venom gland of Polistes snellenitable caption, Table S8: Annotation of top 100 highly expressed genes in the venom gland of Eumenes decoratustable caption, Table S9: Annotation of top 100 highly expressed genes in the venom gland of Sphecidae sp.table caption, Table S10: Annotation of top 100 highly expressed genes in the venom gland of Anterhynchium flavomarginatumtable caption, Table S11: Annotation of top 100 highly expressed genes in the venom gland of Sceliphron deformetable caption, Table S12: Annotation of top 100 highly expressed genes in the venom gland of Bombus ardenstable caption, Table S13: Annotation of top 100 highly expressed genes in the venom gland of Bombus consobrinustable caption, Table S14: Annotation of top 100 highly expressed genes in the venom gland of Bombus ussurensistable caption, Table S15: TPM values of reference housekeeping gene dimethyladenosine transferase in 14 Aculeate bee and wasp speciestable caption, Table S16: Primers used in quantitative real-time PCRtable caption.
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