| Citation: |
YANG Kai-Ning, FU Le-Yi, LI Gui-Li, PU Li-Ping, PAN Hong-Chun. TRANSCRIPTOMIC ANALYSIS OF DIFFERENTIATED RESPONSES BETWEEN SYMBIOTIC AND APOSYMBIOTIC STRAIN OF HYDRA SINENSIS TO POLYSTYRENE NANOPARTICLES[J]. ACTA HYDROBIOLOGICA SINICA, 2024, 48(8): 1333-1347. DOI: 10.7541/2024.2023.0405
|
To investigate the impact of symbiotic algae presence or absence on the tolerance of Hydra sinensis to polystyrene nanoparticles (PS NPs), we conducted a 48h acute toxicity experiment on both symbiotic and aposymbiotic strain of H. sinensis using different PS NPs concentrations (20 nm in diameter). The results showed that the 48h half-lethal concentration (48h LC50) for the symbiotic strain (3.36×102 mg/L) was significantly higher than that of the aposymbiotic strain (1.39×102 mg/L). Subsequently, following exposure to a medium containing 75 mg/L PS NPs for 48h, both symbiotic and aposymbiotic strains underwent transcriptomic analysis, respectively (with a control group having 0 PS NPs). A total of 1532 differentially expressed genes (DEGs) were identified in the symbiotic strain between the PS NPs-treated and control groups, with 763 were up-regulated and 769 down-regulated genes. Similarly, 1079 differentially expressed genes (DEGs) were obtained between PS NPs-treated and control group of the symbiotic strain, with 476 up-regulated and 603 down-regulated genes. KEGG enrichment analysis revealed significant enrichment (P<0.05) of metabolic pathways in both strains, encompassing immune response, pathological indications, material metabolism, cellular processes, organic systems, environmental information processing, and genetic information processing. Among the pathways related to pathological indications, all DEGs were upregulated in only one out of 21 significant pathways for the symbiotic strain, while for the aposymbiotic strain, all DEGs were upregulated in 9 out of 14 significant pathways. This suggests a significantly higher activation level of pathological indicators in the aposymbiotic strain under PS NPs stress compared to the symbiotic strain, indicating a superior tolerance at the molecular level. In addition, all DEGs related to immune response in the aposymbiotic strain treated with PS NPs were upregulated, while only approximately half of the DEGs in the symbiotic strain were upregulated. This suggests a lower immune response sensibility to PS NPs in the symbiotic strain compared to the aposymbiotic strain. In summary, the difference in immune response sensibility to PS NPs between the two H. sinensis strains may underlie their differing tolerance to PS NPs stress at the molecular level. In addition, the symbiotic strain exhibits lower immune response sensitivity to PS NPs, possibly due to the host downregulating immune levels against foreign invaders to accommodate symbiotic algae. The study provides basic data for revealing the biotoxicity and molecular mechanism of nano-sized plastic particles.
| [1] |
Gündoğdu S, Çevik C. Micro-and mesoplastics in Northeast Levantine coast of Turkey: The preliminary results from surface samples [J]. Marine Pollution Bulletin, 2017, 118(1-2): 341-347. doi: 10.1016/j.marpolbul.2017.03.002
|
| [2] |
Rhodes C J. Plastic pollution and potential solutions [J]. Science Progress, 2018, 101(3): 207-260. doi: 10.3184/003685018X15294876706211
|
| [3] |
Akindele E O, Alimba C G. Plastic pollution threat in Africa: current status and implications for aquatic ecosystem health [J]. Environmental Science and Pollution Research International, 2021, 28(7): 7636-7651. doi: 10.1007/s11356-020-11736-6
|
| [4] |
Manfra L, Rotini A, Bergami E, et al. Comparative ecotoxicity of polystyrene nanoparticles in natural seawater and reconstituted seawater using the rotifer Brachionus plicatilis [J]. Ecotoxicology and Environmental Safety, 2017(145): 557-563.
|
| [5] |
Rochman C M, Manzano C, Hentschel B T, et al. Polystyrene plastic: a source and sink for polycyclic aromatic hydrocarbons in the marine environment [J]. Environmental Science & Technology, 2013, 47(24): 13976-13984.
|
| [6] |
Cole M, Lindeque P, Fileman E, et al. Microplastic ingestion by zooplankton [J]. Environmental Science & Technology, 2013, 47(12): 6646-6655.
|
| [7] |
Moore M N. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment [J]? Environment International, 2006, 32(8): 967-976.
|
| [8] |
Kashiwada S. Distribution of nanoparticles in the see-through medaka (Oryzias latipes) [J]. Environmental Health Perspectives, 2006, 114(11): 1697-1702. doi: 10.1289/ehp.9209
|
| [9] |
von Moos N, Burkhardt-Holm P, Köhler A. Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure [J]. Environmental Science & Technology, 2012, 46(20): 11327-11335.
|
| [10] |
Pelley J. Tracking plastics' breakdown products [J]. Environmental Science & Technology, 2008, 42(14): 5035-5036.
|
| [11] |
Bramini M, Ye D, Hallerbach A, et al. Imaging approach to mechanistic study of nanoparticle interactions with the blood-brain barrier [J]. ACS Nano, 2014, 8(5): 4304-4312. doi: 10.1021/nn5018523
|
| [12] |
Wang F, Bexiga M G, Anguissola S, et al. Time resolved study of cell death mechanisms induced by amine-modified polystyrene nanoparticles [J]. Nanoscale, 2013, 5(22): 10868-10876. doi: 10.1039/c3nr03249c
|
| [13] |
Bexiga M G, Varela J A, Wang F, et al. Cationic nanoparticles induce caspase 3-, 7- and 9-mediated cytotoxicity in a human astrocytoma cell line [J]. Nanotoxicology, 2011, 5(4): 557-567. doi: 10.3109/17435390.2010.539713
|
| [14] |
Snell T W, Hicks D G. Assessing toxicity of nanoparticles using Brachionus manjavacas (Rotifera) [J]. Environmental Toxicology, 2011, 26(2): 146-152. doi: 10.1002/tox.20538
|
| [15] |
Ward J E, Kach D J. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves [J]. Marine Environmental Research, 2009, 68(3): 137-142. doi: 10.1016/j.marenvres.2009.05.002
|
| [16] |
Wegner A, Besseling E, Foekema E M, et al. Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.) [J]. Environmental Toxicology and Chemistry, 2012, 31(11): 2490-2497. doi: 10.1002/etc.1984
|
| [17] |
Canesi L, Ciacci C, Bergami E, et al. Evidence for immunomodulation and apoptotic processes induced by cationic polystyrene nanoparticles in the hemocytes of the marine bivalve Mytilus [J]. Marine Environmental Research, 2015(111): 34-40.
|
| [18] |
Cole M, Galloway T S. Ingestion of nanoplastics and microplastics by Pacific oyster larvae [J]. Environmental Science & Technology, 2015, 49(24): 14625-14632.
|
| [19] |
Bergami E, Bocci E, Vannuccini M L, et al. Nano-sized polystyrene affects feeding, behavior and physiology of brine shrimp Artemia franciscana larvae [J]. Ecotoxicology and Environmental Safety, 2016(123): 18-25.
|
| [20] |
Della Torre C, Bergami E, Salvati A, et al. Accumulation and embryotoxicity of polystyrene nanoparticles at early stage of development of sea urchin embryos Paracentrotus lividus [J]. Environmental Science & Technology, 2014, 48(20): 12302-12311.
|
| [21] |
Pardos M, Benninghoff C, Guéguen C, et al. Acute toxicity assessment of Polish (waste) water with a microplate-based Hydra attenuata assay: a comparison with the Microtox test [J]. Science of the Total Environment, 1999(243-244): 141-148.
|
| [22] |
Pascoe D, Karntanut W, Müller C T. Do pharmaceuticals affect freshwater invertebrates? A study with the cnidarian Hydra vulgaris [J]. Chemosphere, 2003, 51(6): 521-528. doi: 10.1016/S0045-6535(02)00860-3
|
| [23] |
Quinn B, Gagné F, Blaise C. Hydra, a model system for environmental studies [J]. The International Journal of Developmental Biology, 2012, 56(6-8): 613-625.
|
| [24] |
Gagné F, Auclair J, Quinn B. Detection of polystyrene nanoplastics in biological samples based on the solvatochromic properties of Nile red: application in Hydra attenuata exposed to nanoplastics [J]. Environmental Science and Pollution Research International, 2019, 26(32): 33524-33531. doi: 10.1007/s11356-019-06501-3
|
| [25] |
Auclair J, Quinn B, Peyrot C, et al. Detection, biophysical effects, and toxicity of polystyrene nanoparticles to the cnidarian Hydra attenuata [J]. Environmental Science and Pollution Research International, 2020, 27(11): 11772-11781. doi: 10.1007/s11356-020-07728-1
|
| [26] |
Auclair J, Gagné F. Crowding effects of polystyrene nanoparticles on lactate dehydrogenase activity in Hydra Attenuata [J]. Journal of Xenobiotics, 2020, 10(1): 2-10. doi: 10.3390/jox10010002
|
| [27] |
潘文健. 中国绿水螅野生型品系及去除共生绿藻品系转录组的初步研究 [D]. 芜湖: 安徽师范大学, 2015: 15-22.
Pan W J. Study on the transcriptome of Hydra sinensis artificial strain without symbiotic algae and its wild type strain [D]. Wuhu: Anhui Normal University, 2015: 15-22.
|
| [28] |
张行, 田晓晓, 董文芳, 等. 中国绿水螅抗坏血酸过氧化物酶基因的克隆、抗体制备及表达分析 [J]. 水生生物学报, 2019, 43(2): 305-314. doi: 10.7541/2019.038
Zhang H, Tian X X, Dong W F, et al. Molecular cloning, antibody preparation and expression analysis of ascorbate peroxidase in Hydra sinensis [J]. Acta Hydrobiologica Sinica, 2019, 43(2): 305-314. doi: 10.7541/2019.038
|
| [29] |
Gao Y, Li A, Zhang W, et al. Assessing the toxicity of bisphenol A and its six alternatives on zebrafish embryo/larvae [J]. Aquatic Toxicology, 2022(246): 106154.
|
| [30] |
Pertea M, Pertea G M, Antonescu C M, et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads [J]. Nature Biotechnology, 2015, 33(3): 290-295. doi: 10.1038/nbt.3122
|
| [31] |
Xing Z, Chu C, Chen L, et al. The use of gene ontology terms and KEGG pathways for analysis and prediction of oncogenes [J]. Biochimica et Biophysica Acta, 2016, 1860(11): 2725-2734. doi: 10.1016/j.bbagen.2016.01.012
|
| [32] |
Maren N A, Duduit J R, Huang D, et al. Stepwise optimization of real-time RT-PCR analysis [J]. Methods in Molecular Biology, 2023(2653): 317-332.
|
| [33] |
Simon L M, Karg S, Westermann A J, et al. MetaMap: an atlas of metatranscriptomic reads in human disease-related RNA-seq data [J]. GigaScience, 2018, 7(6): giy070.
|
| [34] |
Qin W, Gan F, Liang R, et al. Identification of monocyte-associated genes related to the instability of atherosclerosis plaque [J]. Oxidative Medicine and Cellular Longevity, 2022(2022): 3972272.
|
| [35] |
Gu C, Shi X, Dang X, et al. Identification of common genes and pathways in eight fibrosis diseases [J]. Frontiers in Genetics, 2021(11): 627396.
|
| [36] |
Obura D O. Reef corals bleach to resist stress [J]. Marine Pollution Bulletin, 2009, 58(2): 206-212. doi: 10.1016/j.marpolbul.2008.10.002
|
| [37] |
Mohamed A R, Cumbo V, Harii S, et al. The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome [J]. Molecular Ecology, 2016, 25(13): 3127-3141. doi: 10.1111/mec.13659
|
| [38] |
Downs C A, Kramarsky-Winter E, Martinez J, et al. Symbiophagy as a cellular mechanism for coral bleaching [J]. Autophagy, 2009, 5(2): 211-216. doi: 10.4161/auto.5.2.7405
|
| [39] |
Hong M C, Huang Y S, Song P C, et al. Cloning and characterization of ApRab4, a recycling Rab protein of Aiptasia pulchella, and its implication in the symbiosome biogenesis [J]. Marine Biotechnology, 2009, 11(6): 771-785. doi: 10.1007/s10126-009-9193-2
|
| [40] |
Hentschel U, Steinert M, Hacker J. Common molecular mechanisms of symbiosis and pathogenesis [J]. Trends in Microbiology, 2000, 8(5): 226-231. doi: 10.1016/S0966-842X(00)01758-3
|
| [41] |
Bosch T C G. What hydra has to say about the role and origin of symbiotic interactions [J]. The Biological Bulletin, 2012, 223(1): 78-84. doi: 10.1086/BBLv223n1p78
|
| [42] |
Lambert S, Wagner M. Characterisation of nanoplastics during the degradation of polystyrene [J]. Chemosphere, 2016(145): 265-268.
|
| [43] |
Wang H, Ma R, Nienhaus K, et al. Formation of a monolayer protein corona around polystyrene nanoparticles and implications for nanoparticle agglomeration [J]. Small, 2019, 15(22): e1900974. doi: 10.1002/smll.201900974
|
| [44] |
Ding Y, Zhang R, Li B, et al. Tissue distribution of polystyrene nanoplastics in mice and their entry, transport, and cytotoxicity to GES-1 cells [J]. Environmental Pollution, 2021(280): 116974.
|
| [45] |
Revel M, Châtel A, Mouneyrac C. Omics tools: New challenges in aquatic nanotoxicology [J]. Aquatic Toxicology, 2017(193): 72-85.
|
| [46] |
Lin P, Guo Y, He L, et al. Nanoplastics aggravate the toxicity of arsenic to AGS cells by disrupting ABC transporter and cytoskeleton [J]. Ecotoxicology and Environmental Safety, 2021(227): 112885.
|
| [47] |
Girouard M P, Pool M, Alchini R, et al. RhoA proteolysis regulates the actin cytoskeleton in response to oxidative stress [J]. PLoS One, 2016, 11(12): e0168641. doi: 10.1371/journal.pone.0168641
|
| [48] |
Shadab M, Slavin S A, Mahamed Z, et al. Spleen Tyrosine Kinase phosphorylates VE-cadherin to cause endothelial barrier disruption in acute lung injury [J]. The Journal of Biological Chemistry, 2023, 299(12): 105408. doi: 10.1016/j.jbc.2023.105408
|
| [49] |
Bucki R, Levental I, Kulakowska A, et al. Plasma gelsolin: function, prognostic value, and potential therapeutic use [J]. Current Protein & Peptide Science, 2008, 9(6): 541-551.
|
| [50] |
Rauch L, Hennings K, Trasak C, et al. Staphylococcus aureus recruits Cdc42GAP through recycling endosomes and the exocyst to invade human endothelial cells [J]. Journal of Cell Science, 2016, 129(15): 2937-2949.
|
| [51] |
Li Y, Liu Z, Liu B, et al. Citrullinated histone H3: a novel target for the treatment of sepsis [J]. Surgery, 2014, 156(2): 229-234. doi: 10.1016/j.surg.2014.04.009
|
| [52] |
Jawad I, Lukšić I, Rafnsson S B. Assessing available information on the burden of sepsis: global estimates of incidence, prevalence and mortality [J]. Journal of Global Health, 2012, 2(1): 010404.
|
| [53] |
Shinde A, Hardy S D, Kim D, et al. Spleen tyrosine kinase-mediated autophagy is required for epithelial-mesenchymal plasticity and metastasis in breast cancer [J]. Cancer Research, 2019, 79(8): 1831-1843. doi: 10.1158/0008-5472.CAN-18-2636
|
| [54] |
Wang H J, Chen S F, Lo W Y. Identification of cofilin-1 induces G0/G1 arrest and autophagy in angiotensin-(1-7)-treated human aortic endothelial cells from iTRAQ quantitative proteomics [J]. Scientific Reports, 2016(6): 35372.
|
| [55] |
Wang Y, Liu Y, Zhou W, et al. Myosin light-chain kinase inhibitors attenuate nanoparticles-induced autophagy and cytotoxicity by suppression endocytosis [J]. Journal of Nanoscience and Nanotechnology, 2019, 19(7): 3792-3797. doi: 10.1166/jnn.2019.16324
|
| [56] |
Ao X, Zou L, Wu Y. Regulation of autophagy by the Rab GTPase network [J]. Cell Death and Differentiation, 2014, 21(3): 348-358. doi: 10.1038/cdd.2013.187
|
| [57] |
Saurav S, Manna S K. Profilin upregulation induces autophagy through stabilization of AMP-activated protein kinase [J]. FEBS Letters, 2022, 596(14): 1765-1777. doi: 10.1002/1873-3468.14372
|
| [58] |
Chen R H, Chen Y H, Huang T Y. Ubiquitin-mediated regulation of autophagy [J]. Journal of Biomedical Science, 2019, 26(1): 80. doi: 10.1186/s12929-019-0569-y
|
| [59] |
Ye S, Tan C, Yang X, et al. Transcriptome analysis of retinoic acid-inducible gene I overexpression reveals the potential genes for autophagy-related negative regulation [J]. Cells, 2022, 11(13): 2009. doi: 10.3390/cells11132009
|
| [60] |
Li K, Lu M, Cui M, et al. The Notch pathway regulates autophagy after hypoxic-ischemic injury and affects synaptic plasticity [J]. Brain Structure & Function, 2023, 228(3-4): 985-996.
|
| [61] |
Levine B, Kroemer G. Biological functions of autophagy genes: a disease perspective [J]. Cell, 2019, 176(1-2): 11-42. doi: 10.1016/j.cell.2018.09.048
|
| [62] |
Grumati P, Dikic I. Ubiquitin signaling and autophagy [J]. The Journal of Biological Chemistry, 2018, 293(15): 5404-5413. doi: 10.1074/jbc.TM117.000117
|
| [63] |
Abou-Rjeileh U, Contreras G A. Redox regulation of lipid mobilization in adipose tissues [J]. Antioxidants (Basel), 2021, 10(7): 1090. doi: 10.3390/antiox10071090
|
| [64] |
Chu C, Zhang Y, Liu Q, et al. Identification of ceRNA network to explain the mechanism of cognitive dysfunctions induced by PS NPs in mice [J]. Ecotoxicology and Environmental Safety, 2022(241): 113785.
|
| [65] |
Fan X, Wei X, Hu H, et al. Effects of oral administration of polystyrene nanoplastics on plasma glucose metabolism in mice [J]. Chemosphere, 2022, 288(Pt 3): 132607.
|
| [66] |
Xuan L, Wang Y, Qu C, et al. Metabolomics reveals that PS-NPs promote lung injury by regulating prostaglandin B1 through the cGAS-STING pathway [J]. Chemosphere, 2023(342): 140108.
|
| [67] |
Saccà S C, Cutolo C A, Ferrari D, et al. The eye, oxidative damage and polyunsaturated fatty acids [J]. Nutrients, 2018, 10(6): 668. doi: 10.3390/nu10060668
|
| [68] |
Palm W, Sampaio J L, Brankatschk M, et al. Lipoproteins in Drosophila melanogaster-assembly, function, and influence on tissue lipid composition [J]. PLoS Genetics, 2012, 8(7): e1002828. doi: 10.1371/journal.pgen.1002828
|
DownLoad: