Impact of 24-hour hypoxia on hemocyte functions of Anadara kagoshimensis (Tokunaga, 1906)
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Abstract
Shellfish farms are usually located in coastal areas, where molluscs can be exposed to hypoxia. Cultivating at low oxygen levels causes general disruptions of growth rate, outbreaks of diseases, and mollusc mortality. Impact of short-term hypoxia on hemocyte functions of ark clam (Anadara kagoshimensis) was investigated by flow cytometry. A control group was incubated at 6.7–6.8 mg O2·L−1, an experimental one – at 0.4–0.5 mg O2·L−1. Exposition lasted for 24 hours. Hypoxia was created by blowing seawater in shellfish tanks with nitrogen gas. In ark clam hemolymph, 2 groups of hemocytes were identified on the basis of arbitrary size and arbitrary granularity: granulocytes (erythrocytes) and agranulocytes (amebocytes). Erythrocytes were the predominant cell type in A. kagoshimensis hemolymph, amounting for more than 90 %. No significant changes in cellular composition of ark clam hemolymph were observed. The production of reactive oxygen species and hemocyte mortality in the experimental group also remained at control level. The results of this work indicate ark clam tolerance to hypoxia.
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References
Новицкая В. Н., Солдатов А. А. Эритроидные элементы гемолимфы Anadara inaequivalvis (Mollusca: Arcidae) в условиях экспериментальной аноксии: функциональные и морфометрические характеристики. Морской экологический журнал. 2011. Т. 10, № 1. С. 56–64. [Novitskaya V. N., Soldatov A. A. Erythroid elements of hemolymph in Anadara inaequivalvis (Mollusca: Arcidae) under conditions of experimental anoxia: Functional and morphometric characteristics. Morskoj ekologicheskij zhurnal, 2011, vol. 10, no. 1, pp. 56–64. (in Russ.)]
Яхонтова И. В., Дергалева Ж. Т. Марикультура моллюсков на Черноморском побережье России // Рыбпром: технологии и оборудование для переработки водных биоресурсов. 2008. № 2. С. 45–47. [Yakhontova I. V., Dergaleva Zh. T. Marikul’tura mollyuskov na Chernomorskom poberezh’e Rossii. Rybprom: tekhnologii i oborudovanie dlya pererabotki vodnykh bioresursov, 2008, no. 2, pp. 45–47. (in Russ.)]
Andreyeva A. Y., Efremova E. S., Kukhareva T. A. Morphological and functional characterization of hemocytes in cultivated mussel (Mytilus galloprovincialis) and effect of hypoxia on hemocyte parameters. Fish and Shellfish Immunology, 2019, vol. 89, pp. 361–367. https://doi.org/10.1016/j.fsi.2019.04.017
Baker S. M., Mann R. Effects of hypoxia and anoxia on larval settlement, juvenile growth, and juvenile survival of the oyster Crassostrea virginica. The Biological Bulletin, 1992, vol. 182, no. 2, pp. 265–269. https://doi.org/10.2307/1542120
Bao Y., Wang J., Li C., Li P., Wang S., Lin Z. A preliminary study on the antibacterial mechanism of Tegillarca granosa hemoglobin by derived peptides and peroxidase activity. Fish and Shellfish Immunology, 2016, vol. 51, pp. 9–16. https://doi.org/10.1016/j.fsi.2016.02.004
Boyd J. N., Burnett L. E. Reactive oxygen intermediate production by oyster hemocytes exposed to hypoxia. Journal of Experimental Biology, 1999, vol. 202, no. 22, pp. 3135–3143.
Chandel N. S., McClintock D. S., Feliciano C. E., Wood T. M., Melendez J. A., Rodriguez A. M., Schumacker P. T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia a mechanism of O2 sensing. Journal of Biological Chemistry, 2000, vol. 275, no. 33, pp. 25130–25138. https://doi.org/10.1074/jbc.m001914200
Cortesi P., Cattani O., Vitali G., Carpené E., De Zwaan A., Van den Thillart G., Weber R. E. Physiological and biochemical responses of the bivalve Scapharca inaequivalvis to hypoxia and cadmium exposure: Erythrocytes versus other tissues. Marine Coastal Eutrophication, 1992, pp. 1041–1053. https://doi.org/10.1016/B978-0-444-89990-3.50090-0
Dang C., Cribb T. H., Osborne G., Kawasaki M., Bedin A. S., Barnes A. C. Effect of a hemiuroid trematode on the hemocyte immune parameters of the cockle Anadara trapezia. Fish and Shellfish Immunology, 2013, vol. 35, iss. 3, pp. 951–956. https://doi.org/10.1016/j.fsi.2013.07.010
De Zwaan A., Cortesi P., Van den Thillart G., Roos J., Storey K. B. Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: A biochemical analysis. Marine Biology, 1991, vol. 111, no. 3, pp. 343–351. https://doi.org/10.1007/BF01319405
Diaz R. J., Rosenberg R. Spreading dead zones and consequences for marine ecosystems. Science, 2008, vol. 321, iss. 5891, pp. 926–929. https://doi.org/10.1126/science.1156401
Donaghy L., Artigaud S., Sussarellu R., Lambert C., Le Goïc N., Hégaret H., Soudant P. Tolerance of bivalve mollusc hemocytes to variable oxygen availability: A mitochondrial origin? Aquatic Living Resources, 2013, vol. 26, no. 3, pp. 257–261. https://doi.org/10.1051/alr/2013054
Hermes-Lima M., Moreira D. C., Rivera-Ingraham G. A., Giraud-Billoud M., Genaro-Mattos T. C., Campos É. G. Preparation for oxidative stress under hypoxia and metabolic depression: Revisiting the proposal two decades later. Free Radical Biology and Medicine, 2015, vol. 89, pp. 1122–1143. https://doi.org/10.1016/j.freeradbiomed.2015.07.156
Holden J. A., Pipe R. K., Quaglia A., Ciani G. Blood cells of the arcid clam, Scapharca inaequivalvis. Journal of the Marine Biological Association of the United Kingdom, 1994, vol. 74, iss. 2, pp. 287–299. https://doi.org/10.1017/S0025315400039333
Isani G., Cattani O., Tacconi S., Carpene E., Cortesi P. Energy metabolism during anaerobiosis and the recovery of the posterior adductor muscle of Scapharca inaequivalvis. Nova Thalassia, 1986, vol. 8, no. 3, pp. 575–576.
Jiang N., Tan N. S., Ho B., Ding J. L. Respiratory protein–generated reactive oxygen species as an antimicrobial strategy. Nature Immunology, 2007, vol. 8, no. 10, pp. 1114–1122. https://doi.org/10.1038/ni1501
Kawano T., Pinontoan R., Hosoya H., Muto S. Monoamine-dependent production of reactive oxygen species catalyzed by pseudoperoxidase activity of human hemoglobin. Bioscience, Biotechnology, and Biochemistry, 2002, vol. 66, iss. 6, pp. 1224–1232. https://doi.org/10.1271/bbb.66.1224
Miyamoto Y., Iwanaga C. Biochemical responses to anoxia and hypoxia in the ark shell Scapharca kagoshimensis. Plankton and Benthos Research, 2012, vol. 7, iss. 4, pp. 167–174. https://doi.org/10.3800/pbr.7.167
Mydlarz L. D., Jones L. E., Harvell C. D. Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Annual Review of Ecology, Evolution, and Systematics, 2006, vol. 37, pp. 251–288. https://doi.org/10.1146/annurev.ecolsys.37.091305.110103
Nicholson S., Morton B. The hypoxia tolerances of subtidal marine bivalves from Hong Kong. In: The Marine Flora and Fauna of Hong Kong and Southern China V : proceedings of the Tenth International Marine Biological Workshop, Hong Kong, 6–26 Apr., 1998. Hong Kong : Hong Kong University, 2000, pp. 229–239.
Novitskaya V. N., Soldatov A. A. Peculiarities of functional morphology of erythroid elements of hemolymph of the bivalve mollusk Anadara inaequivalvis, the Black Sea. Hydrobiological Journal, 2013, vol. 49, no. 6, pp. 64–71. https://doi.org/10.1615/HydrobJ.v49.i6.60
Soldatov A. A., Sysoeva I. V., Sysoev A. A., Andreyenko T. I. Adenylate system of tissues of the bivalve mollusk Anadara inaequivalvis under experimental anoxia. Hydrobiological Journal, 2010, vol. 46, no. 5, pp. 60–67. https://doi.org/10.1615/HydrobJ.v46.i5.70
Soldatov A. A., Kukhareva T. A., Andreeva A. Y., Efremova E. S. Erythroid elements of hemolymph in Anadara kagoshimensis (Tokunaga, 1906) under conditions of the combined action of hypoxia and hydrogen sulfide contamination. Russian Journal of Marine Biology, 2018, vol. 44, iss. 6, pp. 452–457. https://doi.org/10.1134/S1063074018060111
Sui Y., Kong H., Shang Y., Huang X., Wu F., Hu M., Wang Y. Effects of short-term hypoxia and seawater acidification on hemocyte responses of the mussel Mytilus coruscus. Marine Pollution Bulletin, 2016, vol. 108, iss. 1–2, pp. 46–52. https://doi.org/10.1016/j.marpolbul.2016.05.001
Sussarellu R., Fabioux C., Sanchez M. C., Le Goïc N., Lambert C., Soudant P., Moraga D. Molecular and cellular response to short-term oxygen variations in the Pacific oyster Crassostrea gigas. Journal of Experimental Marine Biology and Ecology, 2012, vol. 412, pp. 87–95. https://doi.org/10.1016/j.jembe.2011.11.007
Sussarellu R., Dudognon T., Fabioux C., Soudant P., Moraga D., Kraffe E., Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster, Crassostrea gigas. Journal of Experimental Biology, 2013, vol. 216, no. 9, pp. 1561–1569. https://doi.org/10.1242/jeb.075879
Sussarellu R., Fabioux C., Le Moullac G., Fleury E., Moraga D. Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Marine Genomics, 2010, vol. 3, no. 3–4, pp. 133–143. https://doi.org/10.1016/j.margen.2010.08.005
Wang Y., Hu M., Cheung S. G., Shin P. K. S., Lu W., Li J. Immune parameter changes of hemocytes in green-lipped mussel Perna viridis exposure to hypoxia and hyposalinity. Aquaculture, 2012, vol. 356, pp. 22–29. https://doi.org/10.1016/j.aquaculture.2012.06.001
Wang W. X., Widdows J. Physiological responses of mussel larvae Mytilus edulis to environmental hypoxia and anoxia. Marine Ecology Progress Series, 1991, vol. 70, no. 3, pp. 223–236.
Widdows J., Newell R. I. E., Mann R. Effects of hypoxia and anoxia on survival, energy metabolism, and feeding of oyster larvae (Crassostrea virginica, Gmelin). The Biological Bulletin, 1989, vol. 177, no. 1, pp. 154–166. https://doi.org/10.2307/1541843
Wu R. S. S. Hypoxia: From molecular responses to ecosystem responses. Marine Pollution Bulletin, 2002, vol. 45, iss. 1–12, pp. 35–45. https://doi.org/10.1016/S0025-326X(02)00061-9
Zwaan A., Isani G., Cattani O., Cortesi P. Long-term anaerobic metabolism of erythrocytes of the arcid clam Scapharca inaequivalvis. Journal of Experimental Marine Biology and Ecology, 1995, vol. 187, iss. 1, pp. 27–37. https://doi.org/10.1016/0022-0981(94)00168-D