Context-dependent antioxidant defense system (ADS)-based stress memory in response to recurrent environmental challenges in congeneric invasive species

Abstract

Marine ecosystems are facing escalating environmental fluctuations owing to climate change and human activities, imposing pressures on marine species. To withstand recurring environmental challenges, marine organisms, especially benthic species lacking behavioral choices to select optimal habitats, have to utilize well-established strategies such as the antioxidant defense system (ADS) to ensure their survival. Therefore, understanding of the mechanisms governing the ADS-based response is essential for gaining insights into adaptive strategies for managing environmental challenges. Here we conducted a comparative analysis of the physiological and transcriptional responses based on the ADS during two rounds of 'hypersalinity-recovery' challenges in two model congeneric invasive ascidians, Ciona robusta and C. savignyi. Our results demonstrated that C. savignyi exhibited higher tolerance and resistance to salinity stresses at the physiological level, while C. robusta demonstrated heightened responses at the transcriptional level. We observed distinct transcriptional responses, particularly in the utilization of two superoxide dismutase (SOD) isoforms. Both Ciona species developed physiological stress memory with elevated total SOD (T-SOD) and glutathione (GSH) responses, while only C. robusta demonstrated transcriptional stress memory. The regulatory distinctions within the Nrf2-Keap1 signalling pathway likely explain the formation disparity of transcriptional stress memory between both Ciona species. These findings support the 'context-dependent stress memory hypothesis', emphasizing the emergence of species-specific stress memory at diverse regulatory levels in response to recurrent environmental challenges. Our results enhance our understanding of the mechanisms of environmental challenge management in marine species, particularly those related to the ADS.

Keywords

Antioxidant defense / Ascidian / Biological invasion / Environmental stress / Stress memory

References

[1] Avramova Z. Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J, 2015, 83: 149-159,

[2] Battino M, Giampieri F, Pistollato F, Sureda A, De Oliveira MR, Pittalà V, Fallarino F, Nabavi SF, Atanasov AG, Nabavi SM. Nrf2 as regulator of innate immunity: a molecular Swiss army knife!. Biotechnol Adv, 2018, 36: 358-370,

[3] Berna L, Alvarez-Valin F, D'Onofrio G. How fast is the sessile Ciona?. Comp Funct Genom, 2009, 2009,

[4] Bhattachan P, Qiao R, Dong B. Identification and population genetic comparison of three ascidian species based on mtDNA sequences. Ecol Evol, 2020, 10: 3758-3768,

[5] Blewett TA, Binning SA, Weinrauch AM, Ivy CM, Rossi GS, Borowiec BG, Lau GY, Overduin SL, Aragao I, Norin T. Physiological and behavioural strategies of aquatic animals living in fluctuating environments. J Exp Biol, 2022, 225: jeb242503,

[6] Briski E, Bailey SA, Casas-Monroy O, DiBacco C, Kaczmarska I, Lawrence JE, Leichsenring J, Levings C, MacGillivary ML, McKindsey CW, Nasmith LE, Parenteau M, Piercey GE, Rivkin RB, Rochon A, Roy S, Simard N, Sun B, Way C, Weise AM, et al.. Taxon- and vector-specific variation in species richness and abundance during the transport stage of biological invasions. Limnol Oceanogr, 2013, 58: 1361-1372,

[7] Brown KT, Barott KL. The costs and benefits of environmental memory for reef-building corals coping with recurring marine heatwaves. Integr Comp Biol, 2022, 62: 1748-1755,

[8] Cao C, Leng Y, Kufe D. Catalase activity is regulated by c-Abl and Arg in the oxidative stress response. J Biol Chem, 2003, 278: 29667-29675,

[9] Carlson SM, Cunningham CJ, Westley PA. Evolutionary rescue in a changing world. Trends Ecol Evol, 2014, 29: 521-530,

[10] Carver CE, Mallet AL, Vercaemer B. . Biological synopsis of the solitary tunicate Ciona intestinalis, 2006 Dartmouth Bedford Institute of Oceanography 22-24

[11] Chen Y, Shenkar N, Ni P, Lin Y, Li S, Zhan A. Rapid microevolution during recent range expansion to harsh environments. BMC Evol Bio, 2018, 18: 187,

[12] Chen B, Zhang W, Niu C, Li W, Jia H, Storey KB. Antioxidant response to acute cold exposure and during recovery in juvenile Chinese soft-shelled turtles (Pelodiscus sinensis). J Exp Biol, 2019, 222: jeb197863,

[13] Cheng J, Li J, Zhang Z, Lu H, Chen G, Yao B, Dong Y, Ma L, Yuan X, Xu J, Zhang Y, Dai W, Yang X, Xue L, Zhang Y, Zhang C, Mauricio R, Peng G, Hu S, Valverde BE, et al.. Autopolyploidy-driven range expansion of a temperate-originated plant to pan-tropic under global change. Ecol Monogr, 2021, 91: 17,

[14] Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv, 2016, 2: 2,

[15] da Silva CRB, Riginos C, Wilson RS. An intertidal fish shows thermal acclimation despite living in a rapidly fluctuating environment. J Comp Physiol B, 2019, 189: 385-398,

[16] Davies KJ. Adaptive homeostasis. Mol Aspects Med, 2016, 49: 1-7,

[17] Delsuc F, Philippe H, Tsagkogeorga G, Simion P, Tilak MK, Turon X, López-Legentil S, Piette J, Lemaire P, Douzery EJP. A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biol, 2018, 16: 39,

[18] Detree C, Gallardo-Escarate C. Single and repetitive microplastics exposures induce immune system modulation and homeostasis alteration in the edible mussel Mytilus galloprovincialis. Fish Shellfish Immunol, 2018, 83: 52-60,

[19] Ding Y, Fromm M, Avramova Z. Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat Commun, 2012, 3: 740,

[20] Fofonoff PW, Ruiz GM, Steves B, Carlton J (2018) National exotic marine and estuarine species information system. http://invasions.si.edu/nemesis. Accessed 15 June 2023

[21] Franchi N, Ferro D, Ballarin L, Santovito G. Transcription of genes involved in glutathione biosynthesis in the solitary tunicate Ciona intestinalis exposed to metals. Aqua Toxicol, 2012, 114–115: 14-22,

[22] Fujikawa T, Munakata T, Kondo S, Satoh N, Wada S. Stress response in the ascidian Ciona intestinalis: transcriptional profiling of genes for the heat shock protein 70 chaperone system under heat stress and endoplasmic reticulum stress. Cell Stress Chaperon, 2010, 15: 193-204,

[23] Georgoulis I, Feidantsis K, Giantsis IA, Kakale A, Boc C, Pörtner HO, Sokolova IM, Michaelidis B. Heat hardening enhances mitochondrial potential for respiration and oxidative defence capacity in the mantle of thermally stressed Mytilus galloprovincialis. Sci Rep, 2021, 11: 17098,

[24] Hackerott S, Martell HA, Eirin-Lopez JM. Coral environmental memory: causes, mechanisms, and consequences for future reefs. Trends Ecol Evol, 2021, 36: 1011-1023,

[25] Han J, Won EJ, Hwang D, Rhee J, Kim I, Lee J. Effect of copper exposure on GST activity and on the expression of four GSTs under oxidative stress condition in the monogonont rotifer, Brachionus koreanus. Comp Biochem Phys C, 2013, 158: 91-100

[26] Hansen BH, Rømma S, Garmo ØA, Pedersen SA, Olsvik PA, Andersen RA. Induction and activity of oxidative stress-related proteins during waterborne Cd/Zn-exposure in brown trout (Salmo trutta). Chemosphere, 2007, 67: 2241-2249,

[27] Hilker M, Schmulling T. Stress priming, memory, and signalling in plants. Plant Cell Environ, 2019, 42: 753-761,

[28] Ho WC, Li DY, Zhu D, Zhang J. Phenotypic plasticity as a long-term memory easing readaptations to ancestral environments. Sci Adv, 2020, 6: eaba3388,

[29] Hofmann GE, Todgham AE. Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol, 2010, 72: 127-145,

[30] Hoshino Z, Nishikawa T. Taxonomic studies of Ciona intestinalis (L.) and its allies. Publ Seto Mar Biol Lab, 1985, 30: 61-79,

[31] Huang X, Gao Y, Jiang B, Zhou Z, Zhan A. Reference gene selection for quantitative gene expression studies during biological invasions: a test on multiple genes and tissues in a model ascidian Ciona savignyi. Gene, 2016, 576: 79-87,

[32] Hughes TP, Kerry JT, Connolly SR, Baird AH, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Jacobson M, Liu G, Pratchett MS, Skirving W, Torda G. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat Clim Change, 2018, 9: 40-43,

[33] Kammer AR, Orczewska JI, O'Brien KM. Oxidative stress is transient and tissue specific during cold acclimation of threespine stickleback. J Exp Biol, 2011, 214: 1248-1256,

[34] Lesser MP. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol, 2006, 68: 253-278,

[35] Li E, Wang S, Li C, Wang X, Chen K, Chen L. Transcriptome sequencing revealed the genes and pathways involved in salinity stress of Chinese mitten crab, Eriocheir sinensis. Physiol Genomics, 2014, 46: 177-190,

[36] Li H, Huang X, Zhan A. Stress memory of recurrent environmental challenges in marine invasive species: Ciona robusta as a case study. Front Physiol, 2020, 11: 94,

[37] Lin Y, Zhan A, Hernandez MR, Paolucci E, MacIsaac HJ, Briski E. Can chlorination of ballast water reduce biological invasions?. J Appl Ecol, 2020, 57: 331-343,

[38] Liu H, Able AJ, Able JA. Priming crops for the future: rewiring stress memory. Trends Plant Sci, 2022, 27: 699-716,

[39] Lukić N, Kukavica B, Davidović-Plavšić B, Hasanagić D, Walter J. Plant stress memory is linked to high levels of anti-oxidative enzymes over several weeks. Environ Exp Bot, 2020, 178,

[40] Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol, 2013, 53: 401-426,

[41] Marino R, Melillo D, Italiani P, Boraschi D. Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut. Front Immunol, 2023, 14: 1176982,

[42] Martin S, Nia W. . Stressors in the marine environment, physiological and ecological responses; societal implications, 2016 Oxford University Press

[43] Melillo D, Marino R, Italiani P, Boraschi D. Innate immune memory in invertebrate metazoans: a critical appraisal. Front Immunol, 2018, 9: 1915,

[44] Moreira A, Figueira E, Soares AM, Freitas R. The effects of arsenic and seawater acidification on antioxidant and biomineralization responses in two closely related Crassostrea species. Sci Total Environ, 2016, 545–546: 569-581,

[45] Mozgova I, Mikulski P, Pecinka A, Farrona S. Alvarez-Venegas R, De-la-Peña C, Casas-Mollano J. Epigenetic mechanisms of abiotic stress response and memory in plants. Epigenetics in plants of agronomic importance: fundamentals and applications, 2019 Cham Springer,

[46] Mu H, Sun J, Fang L, Luan T, Williams GA, Cheung SG, Wong CKC, Qiu J. Genetic basis of differential heat resistance between two species of congeneric freshwater snails: insights from quantitative proteomics and base substitution rate analysis. J Proteome Res, 2015, 14: 4296-4308,

[47] Nandamuri SP, Yourick MR, Carleton KL. Adult plasticity in African cichlids: rapid changes in opsin expression in response to environmental light differences. Mol Ecol, 2017, 26: 6036-6052,

[48] Oberkofler V, Pratx L, Baurle I. Epigenetic regulation of abiotic stress memory: maintaining the good things while they last. Curr Opin Plant Biol, 2021, 61,

[49] Oexle S, Jansen M, Pauwels K, Sommaruga R, Meester LD, Stoks R. Rapid evolution of antioxidant defence in a natural population of Daphnia magna. J Evol Biol, 2016, 29: 1328-1337,

[50] Paiva F, Barco A, Chen Y, Mirzajani A, Chan FT, Lauringson V, Baltazar-Soares M, Zhan A, Bailey SA, Javidpour J, Briski E. Is salinity an obstacle for biological invasions?. Glob Change Biol, 2018, 24: 2708-2720,

[51] Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res, 2001, 29,

[52] Pfennig DW. . Phenotypic plasticity & evolution: causes, consequences, controversies, 2021 Taylor & Francis,

[53] Pickering AM, Vojtovich L, Tower J, Davies KJA. Oxidative stress adaptation with acute, chronic, and repeated stress. Free Radic Biol Med, 2013, 55: 109-118,

[54] Pietsch C. Zearalenone (ZEN) and its influence on regulation of gene expression in carp (Cyprinus carpio L.) liver tissue. Toxins, 2017, 9: E283,

[55] Portner HO, Farrell AP. Ecology. physiology and climate change. Science, 2008, 322: 690-692,

[56] Renborg E, Johannesson K, Havenhand J. Variable salinity tolerance in ascidian larvae is primarily a plastic response to the parental environment. Evol Ecol, 2013, 28: 561-572,

[57] Ristow M. Unraveling the truth about antioxidants: mitohormesis explains ROS-induced health benefits. Nat Med, 2014, 20: 709-711,

[58] Rivera-Ingraham GA, Lignot JH. Osmoregulation, bioenergetics and oxidative stress in coastal marine invertebrates: raising the questions for future research. J Exp Biol, 2017, 220: 1749-1760,

[59] Röhrdanz E, Kahl R. Alterations of antioxidant enzyme expression in response to hydrogen peroxide. Free Radic Biol Med, 1998, 24: 27-38,

[60] Saad GA, Hamed SS, Radwan KH, Radwan EH. Screening of genomic DNA and analysis of heavy metals to identify mutations in the genes of Ciona intestinalis (Linnaeus, 1767) collected from the Mediterranean Sea-Alexandria, Egypt. Sci Res Essays, 2011, 6: 4984-5003

[61] Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol, 2014, 24: R453-462,

[62] Shadel GS, Horvath TL. Mitochondrial ROS signaling in organismal homeostasis. Cell, 2015, 163: 560-569,

[63] Shenkar N, Shmuel Y, Huchon D. The invasive ascidian Ciona robusta recorded from a Red Sea marina. Mar Biodivers, 2018, 48: 2211-2214,

[64] Sies H. Fink G. Chapter 13 - Oxidative stress: eustress and distress in redox homeostasis. Stress: physiology, biochemistry, and pathology, 2019 Academic Press 153-163

[65] Sies H, Berndt C, Jones DP. Oxidative stress. Annu Rev Biochem, 2017, 86: 715-748,

[66] Small KS, Brudno M, Hill MM, Sidow A. Extreme genomic variation in a natural population. Proc Natl Acad Sci USA, 2007, 104: 5698-5703,

[67] Smith K, Thia J, Gemmill CEC, Cary SC, Fidler AE. Barcoding of the cytochrome oxidase I (COI) indicates a recent introduction of Ciona savignyi into New Zealand and provides a rapid method for Ciona species discrimination. Aquat Invasions, 2012, 7: 305-313,

[68] Snell-Rood EC, Kobiela ME, Sikkink KL, Shephard AM. Mechanisms of plastic rescue in novel environments. Annu Rev Ecol Evol S, 2018, 49: 331-354,

[69] Somero GN. The physiology of global change: linking patterns to mechanisms. Ann Rev Mar Sci, 2012, 4: 39-61,

[70] Somero GN. Solutions: how adaptive changes in cellular fluids enable marine life to cope with abiotic stressors. Mar Life Sci Technol, 2022, 4: 389-413,

[71] Sthijns MMJPE, Weseler AR, Bast A, Haenen GRMM. Time in redox adaptation processes: from evolution to hormesis. Int J Mol Sci, 2016, 17: 1649,

[72] Storey KB. Oxidative stress animal adaptation in nature. Braz J Med Biol Res, 1996, 29: 1733

[73] Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering CV. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res, 2019, 47: D607-D613,

[74] Tarallo A, Yagi M, Oikawa S, Agnisola C, D'Onofrio G. Comparative morpho-physiological analysis between Ciona robusta and Ciona savignyi. J Eep Mar Biol Ecol, 2016, 485: 83-87,

[75] Thomas L, Lopez EH, Morikawa MK, Palumbi SR. Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef-building corals. Mol Ecol, 2019, 28: 3371-3382,

[76] Wang X, Wang L, Ren Q, Yin S, Liang F, Jia Y. Two superoxide dismutases (SODs) respond to bacterial challenge identified in the marbled eel Anguilla marmorata. Aquaculture, 2016, 451: 316-325,

[77] Wang X, Zhang X, Chen J, Wang X, Cai J, Zhou Q, Dai T, Cao W, Jiang D. Parental drought-priming enhances tolerance to post-anthesis drought in offspring of wheat. Front Plant Sci, 2018, 9: 261,

[78] Wang W, Wang X, Zhang J, Huang M, Cai J, Zhou Q, Dai T, Jiang D. Salicylic acid and cold priming induce late-spring freezing tolerance by maintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat. Plant Growth Regul, 2019, 90: 109-121,

[79] Wang R, Li Y, Chen R, Du H. Transcriptional memory of different types of genes is generally maintained under various environmental conditions in Saccharomyces cerevisiae. J Genet Genom, 2022, 49: 173-176,

[80] Wesener F, Tietjen B. Primed to be strong, primed to be fast: modeling benefits of microbial stress responses. FEMS Microbiol Ecol, 2019, 95: fiz14,

[81] Xue B, Leibler S. Benefits of phenotypic plasticity for population growth in varying environments. Proc Natl Acad Sci USA, 2018, 115: 12745-12750,

[82] Zhan A, MacIsaac HJ, Cristescu ME. Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol, 2010, 19: 4678-4694,

[83] Zhan A, Briski E, Bock DG, Ghabooli S, Maclsaac HJ. Ascidians as models for studying invasion success. Mar Biol, 2015, 162: 2449-2470,

[84] Zhang Z. KaKs_calculator 3.0: Calculating selective pressure on coding and non-coding sequences. Genom Proteom Bioinf, 2022, 20: 536-540,

[85] Zhang Y, Liao J, Li Z, Yu Y, Zhang J, Li Q, Qu L, Shu W, Chen Y. Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol, 2014, 15: 512,

[86] Zhang W, Niu J, Chen J, Yuan L. Antioxidant responses in hibernating Chinese soft soft-shelled turtle Pelodiscus sinensis hatchlings. Comp Biochem Physiol A, 2017, 204: 9-16,

[87] Zheng J, Zeng L, Shen B, Xu M, Zhu A, Wu C. Antioxidant defenses at transcriptional and enzymatic levels and gene expression of Nrf2-Keap1 signaling molecules in response to acute zinc exposure in the spleen of the large yellow croaker Pseudosciaena crocea. Fish Shellfish Immunol, 2016, 52: 1-8,

[88] Zhou L, Wang S. The bright side of ecological stressors. Trends Ecol Evol, 2023, 38: 568-578,