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Integrative analysis uncovers response mechanism of Pirata subpiraticus to chronic cadmium stress

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Abstract

Soil cadmium (Cd) pollution is global environmental pollution and adversely affects paddy field organisms. Wolf spider grants a new insight to evaluate the toxicity triggered by Cd, yet the impact of chronic Cd exposure on the spider and its molecular mechanism remains unclear. The present study found that the wolf spider Pirata subpiraticus fed with Cd-accumulated flies for 5 weeks presented lower catalase, peroxidase, and acetylcholinesterase activities and higher malonaldehyde content than the control spiders (p < 0.05). An in-depth transcriptomic analysis yielded a total of 5995 differentially expressed genes (DEGs, with 3857 up-regulated and 2138 down-regulated genes) from the comparison, and 19 DEGs encoding three enzymatic indicators were down-regulated. Further enrichment analysis indicated that Cd stress could inhibit the expression of cuticle and chitin-encoding genes via the down-regulation of several key enzymes, such as chitin synthase, glutamine-fructose-6-phosphate transaminase, and chitinase. In addition, our findings suggested that hedgehog and FoxO signaling pathways might play an essential role in regulating survival, cell cycle, and autophagy process in spiders, which were primarily down-regulated under Cd stress. An intensely interactive network displayed that Cd exposure could repress key biological processes in P. subpiraticus, particularly peptide metabolic process and peptide biosynthetic process. To sum up, this integrative investigation confirmed an effective bioindicator for assessing Cd-induced toxicity; provided a mass of genes, proteins, and enzymes for further validation; and granted novel perspectives to uncover the molecular responses of spiders to Cd pollution.

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Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  • Akiyama-Oda Y, Oda H (2020) Hedgehog signaling controls segmentation dynamics and diversity via msx1 in a spider embryo. Sci Adv 6.

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  Google Scholar 

  • Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4:2

    Article  Google Scholar 

  • Briscoe J, Thérond P (2005) Hedgehog signaling: from the Drosophila cuticle to anti-cancer drugs. Dev Cell 8:143–151

    Article  CAS  Google Scholar 

  • Çatav ŞS, Genç TO, Oktay MK, Küçükakyüz K (2020) Cadmium toxicity in wheat: impacts on element contents, antioxidant enzyme activities, oxidative stress, and genotoxicity. Bull Environ Contam Toxicol 104:71–77

    Article  Google Scholar 

  • Chen M, Ye GY, Liu ZC, Fang Q, Hu C, Peng YF, Shelton AM (2009) Analysis of Cry1Ab toxin bioaccumulation in a food chain of Bt rice, an herbivore and a predator. Ecotoxicology 18:230–238

    Article  CAS  Google Scholar 

  • Demontis F, Perrimon N (2010) FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143:813–825

    Article  CAS  Google Scholar 

  • Du Y, Hu XF, Wu XH, Shu Y, Jiang Y, Yan XJ (2013) Affects of mining activities on Cd pollution to the paddy soils and rice grain in Hunan province, Central South China. Environ Monit Assess 185:9843–9856

    Article  CAS  Google Scholar 

  • Foelix RF (2011) Biology of spiders. Oxford University Press, Oxford

  • Fu Z, Xi S (2020) The effects of heavy metals on human metabolism. Toxicol Mech Methods 30:167–176

    Article  CAS  Google Scholar 

  • Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Environ Res Public Health 17.

  • Gobe G, Crane D (2010) Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett 198:49–55

    Article  CAS  Google Scholar 

  • Goldbraikh D, Neufeld D, Eid-Mutlak Y, Lasry I, Gilda JE, Parnis A, Cohen S (2020) USP1 deubiquitinates Akt to inhibit PI3K-Akt-FoxO signaling in muscle during prolonged starvation. EMBO Rep 21:e48791

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • Hendrickx F, Maelfait JP, Langenbick F (2003) Absence of cadmium excretion and high assimilation result in cadmium biomagnification in a wolf spider. Ecotoxicol Environ Saf 55:287–292

    Article  CAS  Google Scholar 

  • Hussain N, Chatterjee SK, Maiti TK, Goswami L, Das S, Deb U, Bhattacharya SS (2021) Metal induced non-metallothionein protein in earthworm: a new pathway for cadmium detoxification in chloragogenous tissue. J Hazard Mater 401:123357

    Article  CAS  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480-484

    Article  CAS  Google Scholar 

  • Khayrova A, Lopatin S, Varlamov V (2021) Obtaining chitin, chitosan and their melanin complexes from insects. Int J Biol Macromol 167:1319–1328

    Article  CAS  Google Scholar 

  • Kier WM (2012) The diversity of hydrostatic skeletons. J Exp Biol 215:1247–1257

    Article  Google Scholar 

  • Kong JH, Siebold C, Rohatgi R (2019) Biochemical mechanisms of vertebrate hedgehog signaling. Development 146.

  • Lv B, Wang J, Zhuo J, Yang H, Yang S, Wang Z, Song Q (2020) Transcriptome sequencing reveals the effects of cadmium toxicity on the cold tolerance of the wolf spider Pirata subpiraticus. Chemosphere 254:126802

    Article  CAS  Google Scholar 

  • Lv B, Wang J, He Y, Zeng Z, Tang YE, Li N, Chen LJ, Wang Z, Song QS (2021) Molecular response uncovers neurotoxicity of Pardosa pseudoannulata exposed to cadmium pressure. Environ Pollut 280:117000

    Article  CAS  Google Scholar 

  • Lv B, Yang HL, Peng YD, Wang J, Zeng Z, Li N, Tang YE, Wang Z, Song QS (2021) Cadmium exposure alters expression of protective enzymes and protein processing genes in venom glands of the wolf spider Pardosa pseudoannulata. Environ Pollut 268:115847

    Article  CAS  Google Scholar 

  • Lv B, Peng Y, Peng YD, Wang Z, Song QS (2022a) Integrated transcriptomics and proteomics provide new insights into the cadmium-induced ovarian toxicity on Pardosa pseudoannulata. Chemosphere, 134255.

  • Lv B, Zhuo JZ, Peng YD, Wang Z (2022b) Comparative analysis of cadmium-induced toxicity and survival responses in the wolf spider Pirata subpiraticus under low-temperature treatment. Environ Sci Pollut Res Int 29:32832–32844

  • Meena RAA, Sathishkumar P, Ameen F, Yusoff ARM, Gu FL (2018) Heavy metal pollution in immobile and mobile components of lentic ecosystems-a review. Environ Sci Pollut Res Int 25:4134–4148

    Article  Google Scholar 

  • Oda H, Akiyama-Oda Y (2020) The common house spider Parasteatoda tepidariorum. EvoDevo 11:6

    Article  CAS  Google Scholar 

  • Perić-Mataruga V, Petković B, Ilijin L, Mrdaković M, Dronjak Čučaković S, Todorović D, Vlahović M (2017) Cadmium and high temperature effects on brain and behaviour of Lymantria dispar L. caterpillars originating from polluted and less-polluted forests. Chemosphere 185:628–636

    Article  Google Scholar 

  • Schmitt-Ney M (2020) The Foxo's advantages of being a family: considerations on function and evolution. Cells 9.

  • Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395–403

    Article  CAS  Google Scholar 

  • Tajiri R (2017) Cuticle itself as a central and dynamic player in shaping cuticle. Curr Opin Insect Sci 19:30–35

    Article  Google Scholar 

  • Tang C, Zhang R, Hu X, Song J, Li B, Ou D, Hu X, Zhao Y (2019) Exogenous spermidine elevating cadmium tolerance in Salix matsudana involves cadmium detoxification and antioxidant defense. Int J Phytoremediation 21:305–315

    Article  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  Google Scholar 

  • Wang J, Lv Z, Lei Z, Chen Z, Lv B, Yang H, Wang Z, Song Q (2019) Expression and functional analysis of cytochrome P450 genes in the wolf spider Pardosa pseudoannulata under cadmium stress. Ecotoxicol Environ Saf 172:19–25

    Article  CAS  Google Scholar 

  • Wang J, Peng X, Yang H, Lv B, Wang Z, Song Q (2020) Mul-tiomics analysis of cadmium stress on the ovarian function of the wolf spider Pardosa pseudoannulata. Chemosphere 248:125904

    Article  CAS  Google Scholar 

  • Wang K, Qiao Y, Li H, Huang C (2020) Use of integrated biomarker response for studying the resistance strategy of the earthworm Metaphire californica in Cd-contaminated field soils in Hunan Province. South China Environ Pollut 260:114056

    Article  CAS  Google Scholar 

  • Wang J, He Y, Peng X, Bo L, Wang Z, Song Q (2021) Characterization of cadmium-responsive transcription factors in wolf spider Pardosa pseudoannulata. Chemosphere 268:129239

    Article  CAS  Google Scholar 

  • Wilczek G, Karcz J, Rost-Roszkowska M, Kędziorski A, Wilczek P, Skowronek M, Wiśniewska K, Kaszuba F, Surmiak K (2019) Evaluation of selected biological properties of the hunting web spider (Steatoda grossa, Theridiidae) in the aspect of short- and long-term exposure to cadmium. Sci Total Environ 656:297–306

    Article  CAS  Google Scholar 

  • Wilczek G, Surmiak K, Wawszczak B, Sajewicz M, Kowalska T, Sindera P, Wiśniewska K, Szulinska E (2019) Effect of long-term cadmium and copper intoxication on the efficiency of ampullate silk glands in false black widow Steatoda grossa (Theridiidae) spiders. Comp Biochem Physiol C Toxicol Pharmacol 224:108564

    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 75:1–6

    Article  Google Scholar 

  • Yang H, Peng Y, Shi Y, Tian J, Wang J, Peng X, Xie C, Xu X, Song Q, Wang Z, Lv Z (2018) Transcriptome assembly and expression profiling of the molecular responses to cadmium toxicity in cerebral ganglia of wolf spider Pardosa pseudoannulata (Araneae: Lycosidae). Ecotoxicology 27:198–208

    Article  CAS  Google Scholar 

  • Yang H, Peng Y, Shi Y, Tian J, Wang J, Song Q, Lv Z, Xie C, Wang Z (2018) Transcriptome analysis provides insights into the immunity function of venom glands in Pardosa pseudoannulata in responses to cadmium toxicity. Environ Sci Pollut Res Int 25:23875–23882

    Article  CAS  Google Scholar 

  • Yang H, Wang Z, Wang J, Lv B, Wu Z, Tian J, Yang J (2021) Cadmium-induced oxidative stress and transcriptome changes in the wolf spider Pirata subpiraticus. Sci Total Environ 785:147364

    Article  CAS  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14

    Article  Google Scholar 

  • Zhang X, Chen D, Zhong T, Zhang X, Cheng M, Li X (2015) Assessment of cadmium (Cd) concentration in arable soil in China. Environ Sci Pollut Res Int 22:4932–4941

    Article  CAS  Google Scholar 

  • Zhang L, Xia Q, Zhou Y, Li J (2019) Endoplasmic reticulum stress and autophagy contribute to cadmium-induced cytotoxicity in retinal pigment epithelial cells. Toxicol Lett 311:105–113

    Article  CAS  Google Scholar 

  • Zhang M, Sun X, Xu J (2020) Heavy metal pollution in the East China Sea: a review. Mar Pollut Bull 159:111473

    Article  CAS  Google Scholar 

  • Zhao Y, Hu X, Liu Y, Dong S, Wen Z, He W, Zhang S, Huang Q, Shi M (2017) ROS signaling under metabolic stress: cross-talk between AMPK and AKT pathway. Mol Cancer 16:79

    Article  Google Scholar 

  • Zhao C, Yu D, He Z, Bao L, Feng L, Chen L, Liu Z, Hu X, Zhang N, Wang T, Fu Y (2021) Endoplasmic reticulum stress-mediated autophagy activation is involved in cadmium-induced ferroptosis of renal tubular epithelial cells. Free Radic Biol Med 175:236–248

    Article  CAS  Google Scholar 

  • Zhou YM, Long SS, Li BY, Huang YY, Li YJ, Yu JY, Du HH, Khan S, Lei M (2020) Enrichment of cadmium in rice (Oryza sativa L.) grown under different exogenous pollution sources. Environ Sci Pollut Res Int 27:44249–44256

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Natural Science Foundation of Hunan Province (2020JJ4427) and Key Project of Education Department of Hunan Province (18A024).

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Authors and Affiliations

  1. College of Resources and Environment, Hunan Agricultural University, Changsha, 410128, China

    Ou-lin Dai, Zi-yan Lei & Zhi Wang

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

    Yuan-de Peng

  3. College of Life Science, Hunan Normal University, Changsha, 410081, China

    Zhi Wang

Authors
  1. Ou-lin Dai
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  2. Zi-yan Lei
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  4. Zhi Wang
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Contributions

Zhi Wang: conceptualization and methodology. Ou-lin Dai: data curation, writing original draft, and visualization. Zi-yan Lei: formal analysis and materials preparation. Yuan-de Peng: supervision.

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Correspondence to Zhi Wang.

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The ethical approval was not required. Materials were unregulated spiders, P. subpiraticus, and insect D. melanogaster.

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Dai, Ol., Lei, Zy., Peng, Yd. et al. Integrative analysis uncovers response mechanism of Pirata subpiraticus to chronic cadmium stress. Environ Sci Pollut Res 29, 90070–90080 (2022). https://doi.org/10.1007/s11356-022-22043-7

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  • DOI: https://doi.org/10.1007/s11356-022-22043-7

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