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Transcriptome analysis reveals the molecular response to cadmium toxicity in P. pseudoannulata

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Abstract

Cadmium (Cd) can be transferred and accumulated in spiders, posing a survival risk to them. To analyze potential biological damage caused by Cd accumulation and relevant detoxification strategies employed by spiders in response to Cd exposure, we conducted transcriptome analysis of the 5th instar spider P. pseudoannulata, a common spider species playing a vital role in natural pest control in agricultural fields of southern China. We obtained 92,778 unigenes with an average length of 1104 bp and identified 302, 655, and 424 differentially expressed genes (DEGs) in the spiders fed with Cd-containing fruit flies for 2, 5, and 8 days, respectively. Results showed that the body mass of Cd-containing P. pseudoannulata were reduced when compared with controls, presumably due to delayed maturation of tissues and organs. Meanwhile, functional analysis of DEGs indicated that Cd may have a negative effect on neural signal transduction and molt cycle of the spider. For defense strategies, detoxification enzymes like glutathione S-transferase (GST), catalase (CAT), superoxide dismutase (SOD), and P450, and typical proteins like heat shock protein and metallothionein were all differentially expressed in response to Cd stress. Besides, innate immune responses like toll-like receptor signaling pathways were also upregulated. Multiple critical Cd-responsive genes involved in biological damage, detoxification, and immune response were identified, providing referable foundation for further research on Cd toxicity to P. pseudoannulata.

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Abbreviations

Cd:

cadmium

bp:

base pair

P. pseudoannulata :

Pardosa pseudoannulata

RNA-Seq:

RNA-sequencing

SOD:

superoxide dismutase

CAT:

catalase

TS-2:

spider fed with Cd-containing fruit fly for 2 days

TS-5:

spider fed with Cd-containing fruit fly for 5 days

TS-8:

spider fed with Cd-containing fruit fly for 8 days

CS:

control spider

FPKM:

reads per kilobase of exon model per million mapped reads

RT-qPCR:

real time quantitative PCR

FDR:

false discovery rate

DEGs:

differential expression genes

ROS:

reactive oxygen species

References

  • Ahmad S (2010) Oxidative stress from environmental pollutants. Arch Insect Biochem 29(2):135–157

    Article  Google Scholar 

  • Anders S, Huber W (2013) Differential expression of RNA-Seq data at the gene level-the DESeq package. Embl

  • Babczynska A, Wilczek G, Szulinska E, Franiel I (2011) Quantitative immunodetection of metallothioneins in relation to metals concentration in spiders from variously polluted areas. Ecotox Environ Saf 74(6):1498–1503

    Article  CAS  Google Scholar 

  • Beaty BJ, Mackie RS, Mattingly KS, Carlson JO, Alfredo RK (2002) The midgut epithelium of aquatic arthropods: a critical target organ in environmental toxicology. Environ Health Persp 110(Suppl 6):911–914

    Article  CAS  Google Scholar 

  • Bondgaard M, Bjerregaard P (2005) Association between cadmium and calcium uptake and distribution during the moult cycle of females shore crabs, Carcinus maenas: an in vivo study. Aquat Toxicol 72:17–28

    Article  CAS  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  CAS  Google Scholar 

  • Eraly D, Hendrickx F, Backeljau T, Bervoets L, Lens L (2011) Direct and indirect effects of metal stress on physiology and life history variation in field populations of a lycosid spider. Ecotox Environ Safe 74:1489–1497

    Article  CAS  Google Scholar 

  • Ferreira JA, Nyangoma SO (2008) A multivariate version of the Benjamini-Hochberg method. J Multivar Anal 99(9):2108–2124

    Article  Google Scholar 

  • Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a review. Environ Monit Assess 187(4):201

    Article  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29(7):644–652

    Article  Google Scholar 

  • Grażyna W, Paweł M (1996) Metal body burdens and detoxifying enzymes in spiders from industrially polluted areas. Fresenius J Anal Chem 354(5–6):643–647

    Google Scholar 

  • Guan D, Mo F, Han Y, Gu W, Zhang M (2015) Digital gene expression profiling (DGE) of cadmium-treated Drosophila melanogaster. Environ Toxicol Phar 39(1):300–306

    Article  CAS  Google Scholar 

  • Hare L (1992) Aquatic insects and trace metals: bioavailability, bioaccumulation, and toxicity. Crit Rev Toxicol 22(5–6):327–369

    Article  CAS  Google Scholar 

  • Hendrickx F, Maelfait JP, Speelmans M, Van Straalen NM (2003) Adaptive reproductive variation along a pollution gradient in a wolf spider. Oecologia 134(2):189–194

    Article  Google Scholar 

  • Hendrickx F, Maelfait JP, Lens L (2008) Effect of metal stress on life history divergence and quantitative genetic architecture in a wolf spider. J Evolution Biol 21(1):183–193

    Article  CAS  Google Scholar 

  • Herpin A, Lelong C, Favrel P (2004) Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev Comp Immunol 28(5):461–485

    Article  CAS  Google Scholar 

  • Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. J Appl Ecol27(2)

  • Hu JL (2016) Effect of Cd on development, fecundity and related enzyme activity of Pardosa pseucoanlate. Dissertation, Hunan Agricultural University

  • Itziou A, Kaloyianni M, Dimitriadis VK (2010) In vivo and in vitro effects of metals in reactive oxygen species production, protein carbonylation, and DNA damage in land snails Eobania vermiculata. Arch Environ Con Tox 60(4):697–707

    Article  Google Scholar 

  • Järup L, Berglund M, Elinder CG et al (1998) Health effects of cadmium exposure-a review of the literature and a risk estimate. Scand J Work Env Hea 24(suppl 1):1–51

    Google Scholar 

  • Joseph A, Zhou D, Fitamant J et al (2012) Protein kinases of the hippo pathway: regulation and substrates. Semin Cell Dev Biol 23(7):770–784

    Article  Google Scholar 

  • Jung MP, Lee JH (2012) Bioaccumulation of heavy metals in the wolf spider, Pardosa astrigera L. Koch (Araneae: Lycosidae). Environ Monit Assess 184:1773–1779

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30

    Article  CAS  Google Scholar 

  • Lavoie M, Le Faucheur S, Fortin C et al (2009) Cadmium detoxification strategies in two phytoplankton species: metal binding by newly synthesized thiolated peptides and metal sequestration in granules. Aquat Toxicol 92(2):65

    Article  CAS  Google Scholar 

  • Liu J, Gao J, Yun Y et al (2013) Bioaccumulation of mercury and its effects on survival, development and web-weaving in the funnel-web spider Agelena labyrinthica, (Araneae: Agelenidae). Bull Environ Contam Toxicol 90(5):558

    Article  CAS  Google Scholar 

  • Li CC, Li GY, Yun YL, Chen J, Zhang ZT, Peng Y (2016a) The effects of cadmium exposure on fitness-related traits and antioxidant responses in the wolf spider, Pardosa pseudoannulata. Bull Environ Contam Toxicol 97(1):31–36

    Article  CAS  Google Scholar 

  • Li CC, Wang Y, Li GY et al (2016b) Transcriptome profiling analysis of wolf spider Pardosa pseudoannulata (Araneae: Lycosidae) after cadmium exposure. Int J Mol Sci 17(12):2033

    Article  Google Scholar 

  • Li M, Xi X, Xiao G, Cheng H, Yang Z, Zhou G, Ye J, Li Z (2014) National multi-purpose regional geochemical survey in China. J Geochem Explor 139(1):21–30

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  • Medesani DA, López Greco LS, Rodríguez EM (2004) Interference of cadmium and copper with the endocrine control of ovarian growth, in the estuarine crab Chasmagnathus granulata. Aquat Toxicol 69(2):165–174

    Article  CAS  Google Scholar 

  • Mendez-Armenta M, Rios C (2007) Cadmium neurotoxicity. Environ Toxicol Phar 23(3):350–358

    Article  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628

    Article  CAS  Google Scholar 

  • Pertea G, Huang X, Liang F et al (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19(5):651

    Article  CAS  Google Scholar 

  • Rani A, Kumar A, Lal A et al (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 24(4):378–399

    Article  CAS  Google Scholar 

  • Riechert SE (1974) Thoughts on the ecological significance of spiders. Bioscience 24(6):352–356

    Article  Google Scholar 

  • Rodríguez EM, Medesani DA, Fingerman M (2007) Endocrine disruption in crustaceans due to pollutants: a review. Comp Biochem Physiol A Mol Integr Physiol 146(4):661–671

    Article  Google Scholar 

  • Rodríguez Moreno PA, Medesani DA, Rodríguez EM (2003) Inhibition of molting by cadmium in the crab Chasmagnathus granulata (Decapoda Brachyura). Aquat Toxicol 64(2):155–164

    Article  Google Scholar 

  • Stalmach M, Wilczek G, Wilczek P, et al (2015) DNA damage in haemocytes and midgut gland cells of Steatoda grossa (Theridiidae) spiders exposed to food contaminated with cadmium Ecotox Environ Safe 113:353–361

    Article  CAS  Google Scholar 

  • Stohs S, Bagchi DE, Bagchi M (2000) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 19(3):201–213

    CAS  Google Scholar 

  • Sun M, Ting Li Y, Liu Y, Chin Lee S, Wang L (2016) Transcriptome assembly and expression profiling of molecular responses to cadmium toxicity in hepatopancreas of the freshwater crab Sinopotamon henanense. Sci Rep-UK 6(1)

  • Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17(1):1

    Article  CAS  Google Scholar 

  • Tatusov R L, Fedorova N D, Jackson J D, et al (2003) The COG database: an updated version includes eukaryotes Bmc Bioinformatics 4(1): 41

  • Tian S, Lu L, Labavitch J, Yang X, He Z, Hu H, Sarangi R, Newville M, Commisso J, Brown P (2011) Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiol 157(4):1914

    Article  CAS  Google Scholar 

  • Wang L, Cui X, Cheng H, Chen F, Wang J, Zhao X, Lin C, Pu X (2015) A review of soil cadmium contamination in China including a health risk assessment. Environ Sci Pollut Res Int 22(21):16441–16452

    Article  CAS  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138

    Article  Google Scholar 

  • Wiedenmann B, Franke WW, Kuhn C et al (1986) Synaptophysin: a marker protein for neuroendocrine cells and neoplasms. Proc Natl Acad Sci U S A 83(10):3500

    Article  CAS  Google Scholar 

  • Wilczek G, Babczynska A, Augustyniak M, Migula P (2004) Relations between metals (Zn, Pb, Cd and Cu) and glutathione-dependent detoxifying enzymes in spiders from a heavy metal pollution gradient. Environ Pollut 132(3):453–461

    Article  CAS  Google Scholar 

  • Wilczek G, Kramarz P, Babczyńska A (2003) Activity of carboxylesterase and glutathione S-transferase in different life-stages of carabid beetle (Poecilus cupreus) exposed to toxic metal concentrations. Comp Biochem Phys C 134(4):501–512

    Google Scholar 

  • Wu YS, Huang SL, Chung HC et al (2017) Bioaccumulation of lead and non-specific immune responses in white shrimp (Litopenaeus vannamei) to Pb exposure. Fish Shellfish Immun 62:116–123

    Article  CAS  Google Scholar 

  • Xu B, Chen S, Luo Y et al (2011) Calcium signaling is involved in cadmium-induced neuronal apoptosis via induction of reactive oxygen species and activation of MAPK/mTOR network. PLoS One 6(4):e19052

    Article  CAS  Google Scholar 

  • Yang H, Peng Y, Tian J, Wang J, Hu J, Wang Z (2016) Spiders as excellent experimental models for investigation of heavy metal impacts on the environment: a review. Environ Earth Sci 75(13)

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(Web Server issue):W293–297

    Article  CAS  Google Scholar 

  • Yuan SS, Lv ZM, Zhu AY et al (2017) Negative effect of chronic cadmium exposure on growth, histology, ultrastructure, antioxidant and innate immune responses in the liver of zebrafish: preventive role of blue light emitting diodes. Ecotox Environ Safe 139:18

    Article  CAS  Google Scholar 

  • Zhang X, Zhong T, Liu L, Ouyang X (2015) Impact of soil heavy metal pollution on food safety in China. PLoS One 10(8):e0135182

    Article  Google Scholar 

  • Zhao WC, Cheng JA, Zhang WJ (2005) Evaluation of the control effects of Pardosa pseudoannulata on Nilaparvata lugens (stål) with a monoclonal antibody. Acta Ecologica Sinica (In Chinese) 25(1):78–82

    Google Scholar 

  • Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey AM, Deacon C, Raab A (2008) High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ Sci Technol 42(13):5008–5013

    Article  CAS  Google Scholar 

  • Zmudzki S, Laskowski R (2012) Biodiversity and structure of spider communities along a metal pollution gradient. Ecotoxicology 21(5):1523–1532

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank the Oebiotech Enterprise (Shanghai) for their technical assistance.

Funding

This work was supported by the Natural Science Foundation of P. R. China (No. 31472017, 31272339), the key projects of Hunan Provincial Science and Technology Department (No. 2014FJ2003), the Planned Science and Technology Project of Hunan Province, China (No. 2015RS4036), the research project of Hunan Provincial Education Department (No. 15C0666), the Agricultural Science and Technology Innovation Program of China (No. CAAS-ASTIP-IBFC), and the postgraduate research projects of Hunan Province, China (CX2017B361).

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Authors and Affiliations

  1. College of Life Sciences, Hunan Normal University, Changsha, 410081, Hunan, China

    Juan Wang, Xianjin Peng, Xiang Xu & Zhi Wang

  2. College of Bioscience and Biotechnology, Hunan Agriculture University, Changsha, 410128, Hunan, China

    Juan Wang, Baoyang Wei, Ting Huang, Huilin Yang, Zhiying Sun & Zhi Wang

  3. Institute of Bast Fiber Crops, Chinese Academy of Agricultural Sciences, Changsha, 410205, Hunan, China

    Yuande Peng & Chunliang Xie

  4. Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510080, China

    Zhiyue Lv

  5. Division of Plant Sciences, University of Missouri, Columbia, MO, 65211, USA

    Qisheng Song

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  1. Juan Wang
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Corresponding authors

Correspondence to Zhi Wang or Zhiyue Lv.

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Ethics approval and consent to participate

The ethical approval was not required. Materials used in this study were unregulated common arthropod spiders, Pardosa pseudoannulata, and insect Drosophila melanogaster.

Competing interests

The authors declare that they have no competing interests.

Additional information

Responsible editor: Philippe Garrigues

Juan Wang and Baoyang Wei are co-first authors.

Electronic supplementary material

Table S1

(DOC 27 kb)

Table S2

The list of DEGs at TS-2, TS-5, and TS-8 (FDR < 0.01, absolute value of Log2foldchange > 2). (XLS 567 kb)

Table S3

GO enrichment analysis for all DEGs (FDR < 0.01). (XLS 146 kb)

Table S4

Differentially expressed genes involved in cuticular protein. (XLS 18 kb)

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Wang, J., Wei, B., Peng, Y. et al. Transcriptome analysis reveals the molecular response to cadmium toxicity in P. pseudoannulata. Environ Sci Pollut Res 25, 34294–34305 (2018). https://doi.org/10.1007/s11356-018-3269-3

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