

FOLLOWUS
1.Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
2.Laoshan Laboratory, Qingdao 266237, China
3.South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
4.CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
5.University of Chinese Academy of Sciences, Beijing 100049, China
lcl@qdio.ac.cn
Received:23 March 2023,
Online First:13 April 2023,
Published:01 March 2024
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ZHOU Li,LI Mengna,ZHONG Zhaoshan,et al.Integrated biomarker response to assess toxic impacts of iron and manganese on deep-sea mussel Gigantidasplatifrons under a deep-sea mining activity scenario[J].Journal of Oceanology and Limnology,2024,42(02):522-532.
ZHOU Li,LI Mengna,ZHONG Zhaoshan,et al.Integrated biomarker response to assess toxic impacts of iron and manganese on deep-sea mussel Gigantidasplatifrons under a deep-sea mining activity scenario[J].Journal of Oceanology and Limnology,2024,42(02):522-532. DOI: 10.1007/s00343-023-3048-y.
Deep-sea mining activities can potentially release metals
which pose a toxicological threat to deep-sea ecosystems. Nevertheless
due to the remoteness and inaccessibility of the deep-sea biosphere
there is insufficient knowledge about the impact of metal exposure on its inhabitants. In this study
deep-sea mussel
Gigantidas
platifrons
a commonly used deep-sea toxicology model organism
was exposed to manganese (100
1 000 µg/L) or iron (500
5 000 µg/L) for 7 d
respectively. Manganese and iron were chosen for their high levels of occurrence within deep-sea deposits. Metal accumulation and a battery of biochemical biomarkers related to antioxidative stress in superoxide dismutase (SOD)
catalase (CAT)
malondialdehyde (MDA); immune function in alkaline phosphatase (AKP)
acid phosphatase (ACP); and energy metabolism in pyruvate kinase (PK) and hexokinase (HK) were assessed in mussel gills. Results showed that deep-sea mussel
G
.
platifrons
exhibited a high capacity to accumulate Mn/Fe. In addition
most tested biochemical parameters were altered by metal exposure
demonstrating that metals could induce oxidative stress
suppress the immune system
and affect energy metabolism of deep-sea mussels. The integrated biomarker response (IBR) approach indicated that the exposure to Mn/Fe had a negative impact on deep-sea mussels
and Mn demonstrated a more harmful impact on deep-sea mussels than Fe. Additionally
SOD and CAT biomarkers had the greatest impact on IBR values in Mn treatments
while ACP and HK were most influential for the low- and high-dose Fe groups
respectively. This study represents the first application of the IBR approach to evaluate the toxicity of metals on deep-sea fauna and serves as a crucial framework for risk assessment of deep-sea mining-associated metal exposure.
Abdel-Tawwab M , Wafeek M . 2017 . Fluctuations in water temperature affected waterborne cadmium toxicity: hematology, anaerobic glucose pathway, and oxidative stress status of Nile tilapia, Oreochromis niloticus (L.) . Aquaculture , 477 : 106 - 111 , https://doi.org/10.1016/j.aquaculture.2017.05.007 https://doi.org/10.1016/j.aquaculture.2017.05.007 .
Abreu I A , Cabelli D E . 2010 . Superoxide dismutases—a review of the metal-associated mechanistic variations . Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics , 1804 ( 2 ): 263 - 274 , https://doi.org/10.1016/j.bbapap.2009.11.005 https://doi.org/10.1016/j.bbapap.2009.11.005 .
Amorim V E , Gonçalves O , Capela R et al . 2020 . Immunological and oxidative stress responses of the bivalve Scrobicularia plana to distinct patterns of heatwaves . Fish & Shellfish Immunology , 106 : 1067 - 1077 , https://doi.org/10.1016/j.fsi.2020.09.024 https://doi.org/10.1016/j.fsi.2020.09.024 .
Beliaeff B , Burgeot T . 2002 . Integrated biomarker response: a useful tool for ecological risk assessment . Environmental Toxicology and Chemistry , 21 ( 6 ): 1316 - 1322 , https://doi.org/10.1002/etc.5620210629 https://doi.org/10.1002/etc.5620210629 .
Broeg K , Lehtonen K K . 2006 . Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach . Marine Pollution Bulletin , 53 ( 8-9 ): 508 - 522 , https://doi.org/10.1016/j.marpolbul.2006.02.004 https://doi.org/10.1016/j.marpolbul.2006.02.004 .
Canesi L , Ciacci C , Piccoli G et al . 1998 . In vitro and in vivo effects of heavy metals on mussel digestive gland hexokinase activity: the role of glutathione . Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology , 120 ( 2 ): 261 - 268 , https://doi.org/10.1016/S0742-8413(98)10004-X https://doi.org/10.1016/S0742-8413(98)10004-X .
Chen Q Q , Lackmann C , Wang W Y et al . 2020 . Microplastics lead to hyperactive swimming behaviour in adult zebrafish . Aquatic Toxicology , 224 : 105521 , https://doi.org/10.1016/j.aquatox.2020.105521 https://doi.org/10.1016/j.aquatox.2020.105521 .
Company R , Serafim A , Bebianno M J et al . 2004 . Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus . Marine Environmental Research , 58 ( 2-5 ): 377 - 381 , https://doi.org/10.1016/j.marenvres.2004.03.083 https://doi.org/10.1016/j.marenvres.2004.03.083 .
Company R , Serafim A , Cosson R et al . 2006 . The effect of cadmium on antioxidant responses and the susceptibility to oxidative stress in the hydrothermal vent mussel Bathymodiolus azoricus . Marine Biology , 148 ( 4 ): 817 - 825 , https://doi.org/10.1007/s00227-005-0116-0 https://doi.org/10.1007/s00227-005-0116-0 .
Crabtree B , Newsholme E A . 1972 . The activities of phosphorylase, hexokinase, phosphofructokinase, lactate dehydrogenase and the glycerol 3-phosphate dehydrogenase in muscles from vertebrates and invertebrates . Biochemical Journal , 126 ( 1 ): 49 - 58 , https://doi.org/10.1042/bj1260049 https://doi.org/10.1042/bj1260049 .
Damiens G , Gnassia-Barelli M , Loquès F et al . 2007 . Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels . Chemosphere , 66 ( 3 ): 574 - 583 , https://doi.org/10.1016/j.chemosphere.2006.05.032 https://doi.org/10.1016/j.chemosphere.2006.05.032 .
dos Santos Carvalho C , Fernandes M N . 2008 . Effect of copper on liver key enzymes of anaerobic glucose metabolism from freshwater tropical fish Prochilodus lineatus . Comparative Biochemistry and Physiology Part A : Molecular & Integrative Physiology , 151 ( 3 ): 437 - 442 , https://doi.org/10.1016/j.cbpa.2007.04.016 https://doi.org/10.1016/j.cbpa.2007.04.016 .
Géret F , Jouan A , Turpin V et al . 2002 . Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster ( Crassostrea gigas ) and the mussel ( Mytilus edulis ) . Aquatic Living Resources , 15 ( 1 ): 61 - 66 , https://doi.org/10.1016/S0990-7440(01)01147-0 https://doi.org/10.1016/S0990-7440(01)01147-0 .
Gollner S , Kaiser S , Menzel L et al . 2017 . Resilience of benthic deep-sea fauna to mining activities . Marine Environmental Research , 129 : 76 - 101 , https://doi.org/10.1016/j.marenvres.2017.04.010 https://doi.org/10.1016/j.marenvres.2017.04.010 .
Góth L . 1991 . A simple method for determination of serum catalase activity and revision of reference range . Clinica Chimica Acta , 196 ( 2-3 ): 143 - 151 , https://doi.org/10.1016/0009-8981(91)90067-M https://doi.org/10.1016/0009-8981(91)90067-M .
Hauton C , Brown A , Thatje S et al . 2017 . Identifying toxic impacts of metals potentially released during deep-sea mining—a synthesis of the challenges to quantifying risk . Frontiers in Marine Science , 4 : 368 , https://doi.org/10.3389/fmars.2017.00368 https://doi.org/10.3389/fmars.2017.00368 . https://do 10.3389/fmars.2017.00368 http://dx.doi.org/10.3389/fmars.2017.00368
Hernroth B , Tassidis H , Baden S P . 2020 . Immunosuppression of aquatic organisms exposed to elevated levels of manganese: From global to molecular perspective . Developmental & Comparative Immunology , 104 : 103536 , https://doi.org/10.1016/j.dci.2019.103536 https://doi.org/10.1016/j.dci.2019.103536 .
Katsikatsou M , Anestis A , Pörtner H O et al . 2011 . Field studies on the relation between the accumulation of heavy metals and metabolic and HSR in the bearded horse mussel Modiolus barbatus . Comparative Biochemistry and Physiology Part C : Toxicology & Pharmacology , 153 ( 1 ): 133 - 140 , https://doi.org/10.1016/j.cbpc.2010.10.001 https://doi.org/10.1016/j.cbpc.2010.10.001 .
Khan F U , Chen H , Gu H X et al . 2021 . Antioxidant responses of the mussel Mytilus coruscus co-exposed to ocean acidification, hypoxia and warming . Marine Pollution Bulletin , 162 : 111869 , https://doi.org/10.1016/j.marpolbul.2020.111869 https://doi.org/10.1016/j.marpolbul.2020.111869 .
Kim W K , Lee S K , Jung J . 2010 . Integrated assessment of biomarker responses in common carp ( Cyprinus carpio ) exposed to perfluorinated organic compounds . Journal of Hazardous Materials , 180 ( 1-3 ): 395 - 400 , https://doi.org/10.1016/j.jhazmat.2010.04.044 https://doi.org/10.1016/j.jhazmat.2010.04.044 .
Kim B M , Rhee J S , Jeong C B et al . 2014 . Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus . Comparative Biochemistry and Physiology Part C : Toxicology & Pharmacology , 166 : 65 - 74 , https://doi.org/10.1016/j.cbpc.2014.07.005 https://doi.org/10.1016/j.cbpc.2014.07.005 .
King J . 1965 . The hydrolases-acid and alkaline phosphatases . In: King J ed. Practical Clinical Enzymology. D. Van Nostrand Company Ltd ., London , p. 191 - 208 .
Laming S R , Gaudron S M , Duperron S . 2018 . Lifecycle ecology of deep-sea chemosymbiotic mussels: a review . Frontiers in Marine Science , 5 : 282 , https://doi.org/10.3389/fmars.2018.00282 https://doi.org/10.3389/fmars.2018.00282 .
Lan W G , Wong M K , Chen N et al . 1995 . Effect of combined copper, zinc, chromium and selenium by orthogonal array design on alkaline phosphatase activity in liver of the red sea bream, Chrysophrys major . Aquaculture , 131 ( 3-4 ): 219 - 230 , https://doi.org/10.1016/0044-8486(94)00326-J https://doi.org/10.1016/0044-8486(94)00326-J .
Li Y M , Liu Z Q , Li M F et al . 2020 . Effects of nanoplastics on antioxidant and immune enzyme activities and related gene expression in juvenile Macrobrachium nipponense . Journal of Hazardous Materials , 398 : 122990 , https://doi.org/10.1016/j.jhazmat.2020.122990 https://doi.org/10.1016/j.jhazmat.2020.122990 .
Li Y M , Liu Z Q , Yang Y et al . 2021a . Effects of nanoplastics on energy metabolism in the oriental river prawn ( Macrobrachium nipponense ) . Environmental Pollution , 268 : 115890 , https://doi.org/10.1016/j.envpol.2020.115890 https://doi.org/10.1016/j.envpol.2020.115890 .
Li Y X , Men B , He Y et al . 2017 . Effect of single-wall carbon nanotubes on bioconcentration and toxicity of perfluorooctane sulfonate in zebrafish ( Danio rerio ) . Science of the Total Environment , 607 - 608 : 509 - 518 , https://doi.org/10.1016/j.scitotenv.2017.06.140 https://doi.org/10.1016/j.scitotenv.2017.06.140 .
Li Z H , Li P , Wu Y . 2021b . Effects of waterborne mercury at different temperatures on hematology and energy metabolism in grass carp ( Ctenopharyngodon idella ) . International Journal of Environmental Science and Technology , 18 ( 6 ): 1489 - 1498 , https://doi.org/10.1007/s13762-020-02906-7 https://doi.org/10.1007/s13762-020-02906-7 .
Livingstone D R . 2001 . Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms . Marine Pollution Bulletin , 42 ( 8 ): 656 - 666 , https://doi.org/10.1016/S0025-326X(01)00060-1 https://doi.org/10.1016/S0025-326X(01)00060-1 .
Lovett D L , Towle D W , Faris J E . 1994 . Salinity-sensitive alkaline phosphatase activity in gills of the blue crab, Callinectes sapidus Rathbun . Comparative Biochemistry and Physiology Part B: Comparative Biochemistry , 109 ( 1 ): 163 - 173 , https://doi.org/10.1016/0305-0491(94)90153-8 https://doi.org/10.1016/0305-0491(94)90153-8 .
Malcovati M , Valentini G . 1982 . AMP-and fructose 1, 6-bisphosphate-activated pyruvate kinases from Escherichia coli . Methods in Enzymology , 90 : 170 - 179 , https://doi.org/10.1016/S0076-6879(82)90123-9 https://doi.org/10.1016/S0076-6879(82)90123-9 .
Martins I , Goulart J , Martins E et al . 2017 . Physiological impacts of acute Cu exposure on deep-sea vent mussel Bathymodiolus azoricus under a deep-sea mining activity scenario . Aquatic Toxicology , 193 : 40 - 49 , https://doi.org/10.1016/j.aquatox.2017.10.004 https://doi.org/10.1016/j.aquatox.2017.10.004 .
Mazorra M T , Rubio J A , Blasco J . 2002 . Acid and alkaline phosphatase activities in the clam Scrobicularia plana : kinetic characteristics and effects of heavy metals . Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology , 131 ( 2 ): 241 - 249 , https://doi.org/10.1016/S1096-4959(01)00502-4 https://doi.org/10.1016/S1096-4959(01)00502-4 .
McCord J M , Fridovich I . 1969 . Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) . Journal of Biological Chemistry , 244 ( 22 ): 6049 - 6055 , https://doi.org/10.1016/S0021-9258(18)63504-5 https://doi.org/10.1016/S0021-9258(18)63504-5 .
O'Neal S L , Zheng W . 2015 . Manganese toxicity upon overexposure: a decade in review . Current Environmental Health Reports , 2 ( 3 ): 315 - 328 , https://doi.org/10.1007/s40572-015-0056-x https://doi.org/10.1007/s40572-015-0056-x .
Rajalakshmi S , Mohandas A . 2005 . Copper-induced changes in tissue enzyme activity in a freshwater mussel . Ecotoxicology and Environmental Safety , 62 ( 1 ): 140 - 143 , https://doi.org/10.1016/j.ecoenv.2005.01.003 https://doi.org/10.1016/j.ecoenv.2005.01.003 .
Roberts D A . 2012 . Causes and ecological effects of resuspended contaminated sediments (RCS) in marine environments . Environment International , 40 : 230 - 243 , https://doi.org/10.1016/j.envint.2011.11.013 https://doi.org/10.1016/j.envint.2011.11.013 .
Roméo M , Bennani N , Gnassia-Barelli M et al . 2000 . Cadmium and copper display different responses towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax . Aquatic Toxicology , 48 ( 2-3 ): 185 - 194 , https://doi.org/10.1016/S0166-445X(99)00039-9 https://doi.org/10.1016/S0166-445X(99)00039-9 .
Ruiz P , Katsumiti A , Nieto J A et al . 2015 . Short-term effects on antioxidant enzymes and long-term genotoxic and carcinogenic potential of CuO nanoparticles compared to bulk CuO and ionic copper in mussels Mytilus galloprovincialis . Marine Environmental Research , 111 : 107 - 120 , https://doi.org/10.1016/j.marenvres.2015.07.018 https://doi.org/10.1016/j.marenvres.2015.07.018 .
Sanchez W , Burgeot T , Porcher J M . 2013 . A novel "Integrated Biomarker Response" calculation based on reference deviation concept . Environmental Science and Pollution Research , 20 ( 5 ): 2721 - 2725 , https://doi.org/10.1007/s11356-012-1359-1 https://doi.org/10.1007/s11356-012-1359-1 . https://do 10.1007/s11356-012-1359-1 http://dx.doi.org/10.1007/s11356-012-1359-1
Santos M M , Jorge P A S , Coimbra J et al . 2018 . The last frontier: coupling technological developments with scientific challenges to improve hazard assessment of deep-sea mining . Science of the Total Environment , 627 : 1505 - 1514 , https://doi.org/10.1016/j.scitotenv.2018.01.221 https://doi.org/10.1016/j.scitotenv.2018.01.221 .
Satyanarayana U . 2021 . Biochemistry, 6e-E-book. 6 th edn . Elsevier Health Sciences, New York .
Sedlak J , Lindsay R H . 1968 . Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent . Analytical Biochemistry , 25 : 192 - 205 . https://do 10.1016/0003-2697(68)90092-4 http://dx.doi.org/10.1016/0003-2697(68)90092-4
Shanmuganathan A , Avery S V , Willetts S A et al . 2004 . Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway . FEBS Letters , 556 ( 1-3 ): 253 - 259 , https://doi.org/10.1016/S0014-5793(03)01428-5 https://doi.org/10.1016/S0014-5793(03)01428-5 .
Sokolova I M , Frederich M , Bagwe R et al . 2012 . Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates . Marine Environmental Research , 79 : 1 - 15 , https://doi.org/10.1016/j.marenvres.2012.04.003 https://doi.org/10.1016/j.marenvres.2012.04.003 .
Uchiyama M , Mihara M . 1978 . Determination of malonaldehyde precursor in tissues by thiobarbituric acid test . Analytical biochemistry , 86 ( 1 ): 271 - 278 , https://doi.org/10.1016/0003-2697(78)90342-1 https://doi.org/10.1016/0003-2697(78)90342-1 .
Valko M , Morris H , Cronin M T D . 2005 . Metals, toxicity and oxidative stress . Current Medicinal Chemistry , 12 ( 10 ): 1161 - 1208 , https://doi.org/10.2174/0929867053764635 https://doi.org/10.2174/0929867053764635 .
Valkova E , Atanasov V , Veleva P . 2020 . Content of Fe and Mn in waters and zebra mussel ( Dressena polymorpha ) from Ovcharitsa Dam, Stara Zagora region, Bulgaria . Bulgarian Journal of Agricultural Science , 26 ( 4 ): 870 - 876 .
Viarengo A , Nott J A . 1993 . Mechanisms of heavy metal cation homeostasis in marine invertebrates . Comparative Biochemistry and Physiology Part C: Comparative Pharmacology , 104 ( 3 ): 355 - 372 , https://doi.org/10.1016/0742-8413(93)90001-2 https://doi.org/10.1016/0742-8413(93)90001-2 . https://do 10.1016/0742-8413(93)90001-2 http://dx.doi.org/10.1016/0742-8413(93)90001-2
Wang X , Li P , He S W et al . 2022 . Effects of tralopyril on histological, biochemical and molecular impacts in Pacific oyster, Crassostrea gigas . Chemosphere , 289 : 133157 , https://doi.org/10.1016/j.chemosphere.2021.133157 https://doi.org/10.1016/j.chemosphere.2021.133157 .
Wang X C , Li C L , Zhou L . 2017 . Metal concentrations in the mussel Bathymodiolus platifrons from a cold seep in the South China Sea . Deep Sea Research Part I: Oceanographic Research Papers , 129 : 80 - 88 , https://doi.org/10.1016/j.dsr.2017.10.004 https://doi.org/10.1016/j.dsr.2017.10.004 .
Yu J C , Xiao Y S , Wang Y F et al . 2021 . Chronic nitrate exposure cause alteration of blood physiological parameters, redox status and apoptosis of juvenile turbot ( Scophthalmus maximus ) . Environmental Pollution , 283 : 117103 , https://doi.org/10.1016/j.envpol.2021.117103 https://doi.org/10.1016/j.envpol.2021.117103 .
Zeng Z G . 2011 . Submarine Hydrothermal Geology . Science Press , Beijing . (in Chinese)
Zhou L , Cao L , Wang X C et al . 2020 . Metal adaptation strategies of deep-sea Bathymodiolus mussels from a cold seep and three hydrothermal vents in the West Pacific . Science of the Total Environment , 707 : 136046 , https://doi.org/10.1016/j.scitotenv.2019.136046 https://doi.org/10.1016/j.scitotenv.2019.136046 .
Zhou L , Li M N , Zhong Z S et al . 2021 . Biochemical and metabolic responses of the deep-sea mussel Bathymodiolus platifrons to cadmium and copper exposure . Aquatic Toxicology , 236 : 105845 , https://doi.org/10.1016/j.aquatox.2021.105845 https://doi.org/10.1016/j.aquatox.2021.105845 .
Zhou L , Li M N , Zhong Z S et al . 2023 . Toxicological effects of cadmium on deep-sea mussel Gigantidas platifrons revealed by a combined proteomic and metabolomic approach . Frontiers in Marine Science , 10 : 1087411 , https://doi.org/10.3389/fmars.2023.1087411 https://doi.org/10.3389/fmars.2023.1087411 .
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