Effect of static magnetic field on marine mollusc Elysia leucolegnote

Artificial magnetic fields are unavoidable environment for offshore marine organisms. With the substantially increasing submarine cables, the impact of magnetic field generated by cables on marine organisms has gradually attracted people’s attention. However, there are few studies on the effect of magnetic field on molluscs. To explore whether magnetic fields could interfere with the physiological functions of offshore molluscs, here we systematically analyzed the change of metabolism and transcriptome of Elysia leucolegnote exposed to either geomagnetic field or 1.1 T static magnetic field. The blood glucose and lipid levels, as well as the activities of antioxidant enzymes in E. leucolegnote were significantly increased upon the exposure to high static magnetic field for 10 days. Meanwhile, the activities of enzymes related to digestive performance and liver functions were decreased. Possible mechanisms were further revealed through comparative transcriptome analysis. A total of 836 differentially expressed genes were identified, 352 of which were up-regulated and 484 of which were down-regulated after exposure to the high static magnetic field. The up-regulated differential genes were mainly concentrated in lysosomal and apoptotic pathways, and down-regulated differential genes were mainly involved in digestive and immune systems including phagocytosis. This pattern was further confirmed by RT-qPCR analysis. In conclusion, prolonged exposure to a 1.1 T static magnetic field increased oxidative stress and blood glucose and lipid levels, and decreased immunity and physiological conditions in E. leucolegnote. The data we presented here provides a comprehensive view of metabolism change and gene expression pattern of E. leucolegnote exposed to static magnetic field. It may expand our knowledge on the magnetic field effects on offshore mollusc at molecular level, and contribute to clarification of the interaction between marine animals and artificial magnetic fields, which is certainly ecologically important.

[1]  S. Tofani.  Magnetic fields and apoptosis: a possible mechanism , 2022, Electromagnetic biology and medicine.

[2]  Can Xie.  Searching for unity in diversity of animal magnetoreception: From biology to quantum mechanics and back , 2022, Innovation.

[3]  A. Lyndon,et al.  Exposure to Electromagnetic Fields (EMF) from Submarine Power Cables Can Trigger Strength-Dependent Behavioural and Physiological Responses in Edible Crab, Cancer pagurus (L.) , 2021, Journal of Marine Science and Engineering.

[4]  Felipe A. Simão,et al.  BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes , 2021, Molecular biology and evolution.

[5]  I. Golovanova,et al.  Long-Term Consequences of the Effect of Copper and an Electromagnetic Field on the Size and Weight Parameters and Activity of Digestive Glycosidases in Underyearlings of Roach Rutilus rutilus , 2021, Inland Water Biology.

[6]  J. M. Torta,et al.  International Geomagnetic Reference Field: the thirteenth generation , 2021, Earth, Planets and Space.

[7]  Xin Zhang,et al.  A Static Magnetic Field Improves Iron Metabolism and Prevents High-Fat-Diet/Streptozocin-Induced Diabetes , 2021, Innovation.

[8]  P. Oliver,et al.  ROS Generation in Microglia: Understanding Oxidative Stress and Inflammation in Neurodegenerative Disease , 2020, Antioxidants.

[9]  Yutaka Suzuki,et al.  Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus , 2020, bioRxiv.

[10]  Y. Liu,et al.  Effects of supplemental ultraviolet light on growth, oxidative stress responses, and apoptosis-related gene expression of the shrimp Litopenaeus vannamei , 2020 .

[11]  Y. Liu,et al.  Effect of spectral composition on growth, oxidative stress responses, and apoptosis-related gene expression of the shrimp, Penaeus vannamei , 2020 .

[12]  Zhi Luo,et al.  Nano-Zn Increased Zn Accumulation and Triglyceride Content by Up-Regulating Lipogenesis in Freshwater Teleost, Yellow Catfish Pelteobagrus fulvidraco , 2020, International journal of molecular sciences.

[13]  Mingming Zhang,et al.  Immune response of molluscs Onchidium struma to extremely low-frequency electromagnetic fields (ELF-EMF, 50 Hz) exposure based on immune-related enzyme activity and De novo transcriptome analysis. , 2020, Fish & shellfish immunology.

[14]  D. Nyqvist,et al.  Electric and magnetic senses in marine animals, and potential behavioral effects of electromagnetic surveys. , 2020, Marine environmental research.

[15]  Y. Wardiatno.  New distribution record of Elysia leucolegnote (Jensen, 1990) (Sacoglossa Plakobranchidae) in mangrove ecosystem of Biak Numfor, Papua - Indonesia , 2020 .

[16]  E. Andrulewicz,et al.  Effect of low frequency electromagnetic field on the behavior and bioenergetics of the polychaete Hediste diversicolor. , 2019, Marine environmental research.

[17]  D. P. Fey,et al.  Are magnetic and electromagnetic fields of anthropogenic origin potential threats to early life stages of fish? , 2019, Aquatic toxicology.

[18]  D. P. Fey,et al.  Genotoxic and cytotoxic effects of 50 Hz 1 mT electromagnetic field on larval rainbow trout (Oncorhynchus mykiss), Baltic clam (Limecola balthica) and common ragworm (Hediste diversicolor). , 2019, Aquatic toxicology.

[19]  Juan Bald,et al.  A review of potential impacts of submarine power cables on the marine environment: Knowledge gaps, recommendations and future directions , 2018, Renewable and Sustainable Energy Reviews.

[20]  H. Mouritsen.  Long-distance navigation and magnetoreception in migratory animals , 2018, Nature.

[21]  M. M. Khoshroo,et al.  Some immunological responses of common carp (Cyprinus carpio) fingerling to acute extremely low-frequency electromagnetic fields (50 Hz) , 2018, Fish Physiology and Biochemistry.

[22]  Huizhen Wang,et al.  Magnetic Fields and Reactive Oxygen Species , 2017, International journal of molecular sciences.

[23]  Yan Wang,et al.  Effect of blood glucose level on acute stress response of grass carp Ctenopharyngodon idella , 2017, Fish Physiology and Biochemistry.

[24]  Claire B Paris-Limouzy,et al.  Glass eels (Anguilla anguilla) have a magnetic compass linked to the tidal cycle , 2017, Science Advances.

[25]  K. Lohmann,et al.  Effect of magnetic pulses on Caribbean spiny lobsters: implications for magnetoreception , 2016, Journal of Experimental Biology.

[26]  L. Dini,et al.  Early Development of Sea Urchin P.lividus Under Static (6 mT) and Pulsed Magnetic Fields (15 and 72 Hz) , 2016 .

[27]  Taijiao Jiang,et al.  A magnetic protein biocompass. , 2016, Nature materials.

[28]  Zhang Hu,et al.  Effects of magnetic field of offshore wind farm on the survival and behavior of marine organisms , 2016 .

[29]  S. Kelly,et al.  TransRate: reference-free quality assessment of de novo transcriptome assemblies , 2015, bioRxiv.

[30]  N. V. Ushakova,et al.  The effect of magnetic fields on the activity of proteinases and glycosidases in the intestine of the crucian carp Carassius carassius , 2015, Biology Bulletin.

[31]  B. Heidari,et al.  The physiological responses of the Caspian kutum (Rutilus frisii kutum) fry to the static magnetic fields with different intensities during acute and subacute exposures. , 2015, Ecotoxicology and environmental safety.

[32]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[33]  I. Golovanova,et al.  Effect of a magnetic field and copper upon activity of hydrolytic enzymes in roach (Rutilus rutilus) underyearlings , 2013, Journal of Ichthyology.

[34]  Y. Kubo,et al.  Zebrafish respond to the geomagnetic field by bimodal and group-dependent orientation , 2012, Scientific Reports.

[35]  Zhengwei Zhu,et al.  CD-HIT: accelerated for clustering the next-generation sequencing data , 2012, Bioinform..

[36]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[37]  Chuan-Yun Li,et al.  KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases , 2011, Nucleic Acids Res..

[38]  S. Fuller-Espie,et al.  Alteration of mitochondrial membrane potential (∆Ψm) and phosphatidylserine translocation as early indicators of heavy metal-induced apoptosis in the earthworm Eisenia hortensis , 2011 .

[39]  N. Friedman,et al.  Trinity : reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2016 .

[40]  C. Swennen.  LARGE MANGROVE-DWELLING ELYSIA SPECIES IN ASIA, WITH DESCRIPTIONS OF TWO NEW SPECIES (GASTROPODA: OPISTOBRANCHIA: SACOGLOSSA) , 2011 .

[41]  Sevil Zencir,et al.  Oxidative Stress and Apoptosis in Relation to Exposure to Magnetic Field , 2011, Cell Biochemistry and Biophysics.

[42]  D. Bhattacharya,et al.  Molecular characterization of the Calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. , 2009, Molecular plant.

[43]  Sönke Johnsen,et al.  Magnetoreception in animals , 2008 .

[44]  Simon Benhamou,et al.  Marine Turtles Use Geomagnetic Cues during Open-Sea Homing , 2007, Current Biology.

[45]  G. Kawamura,et al.  Anguilla japonica is already magnetosensitive at the glass eel phase , 2005 .

[46]  Kenneth J Lohmann,et al.  Magnetic Orientation and Navigation in Marine Turtles, Lobsters, and Molluscs: Concepts and Conundrums1 , 2005, Integrative and comparative biology.

[47]  R. Bochert,et al.  Long‐term exposure of several marine benthic animals to static magnetic fields , 2004, Bioelectromagnetics.

[48]  M. Yashin,et al.  Effect of Rotating Electromagnetic Fields on Proteolytic Activity of Pepsin in Rats , 2004, Bulletin of Experimental Biology and Medicine.

[49]  M. Dębowski,et al.  Effect of a constant magnetic field on water quality and rearing of European sheatfish Silurus glanis L. larvae , 2004 .

[50]  T. Quinn.  Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry , 1980, Journal of comparative physiology.

[51]  Huang Jin-tian.  The observation on ecological habits of Onchidium struma , 2004 .

[52]  L. Boles,et al.  True navigation and magnetic maps in spiny lobsters , 2003, Nature.

[53]  V. Turk,et al.  Apoptotic Pathways: Involvement of Lysosomal Proteases , 2002, Biological chemistry.

[54]  J. Valles.  Model of magnetic field-induced mitotic apparatus reorientation in frog eggs. , 2002, Biophysical journal.

[55]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[56]  S. Tofani,et al.  Static and ELF magnetic fields induce tumor growth inhibition and apoptosis , 2001, Bioelectromagnetics.

[57]  Ishisaka,et al.  Effects of a magnetic fields on the various functions of subcellular organelles and cells. , 2000, Pathophysiology : the official journal of the International Society for Pathophysiology.

[58]  N. W. Pankhurst,et al.  Evaluation of Simple Instruments for the Measurement of Blood Glucose and Lactate, and Plasma Protein as Stress Indicators in Fish , 1999 .

[59]  J. Denegre,et al.  Cleavage planes in frog eggs are altered by strong magnetic fields. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[60]  K. Formicki,et al.  Reactions of fish embryos and larvae to constant magnetic fields , 1998 .

[61]  A O Willows,et al.  Lunar-modulated geomagnetic orientation by a marine mollusk. , 1987, Science.