ВЛИЯНИЕ КРАТКОСРОЧНОЙ РАНЖИРОВАННОЙ ГИПОКСИИ НА ФУНКЦИОНАЛЬНЫЕ И МОРФОЛОГИЧЕСКИЕ ПОКАЗАТЕЛИ ГЕМОЦИТОВ ТИХООКЕАНСКОЙ УСТРИЦЫ CRASSOSTREA GIGAS (THUNBERG, 1793)
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Ключевые слова

устрицы
гипоксия
иммунитет
гемоциты
активные формы кислорода

Аннотация

При помощи методов проточной цитометрии и световой микроскопии исследовано влияние краткосрочной ранжированной гипоксии на морфофункциональные показатели гемоцитов тихоокеанской устрицы (Crassostrea gigas). Контрольная группа содержалась в течение 24 ч при 100 % уровне насыщения воды кислородом, экспериментальные животные – при умеренной (30 % насыщение кислородом) и глубокой гипоксической нагрузке (3 % насыщение кислородом). В гемолимфе устриц идентифицировано три типа клеток – амебоциты, гиалиноциты и гранулоциты. Показано, что гипоксия не оказывала влияния на морфометрические характеристики гемоцитов, однако, индуцировала существенные изменения в функциональных параметрах клеток и приводила к сдвигам клеточного состава гемолимфы. У устриц, содержащихся в условиях умеренного дефицита кислорода, зафиксировано развитие компенсаторного ответа на гипоксию: увеличение числа гранулоцитов на 20%, усиление спонтанной продукции активных форм кислорода (АФК) агранулоцитов (на 40%) и гранулоцитов (на 90%). Глубокая кратковременная гипоксия достоверно ингибировала способность гемоцитов к генерации окислительного взрыва и индуцировала снижение относительного числа гранулярных клеток (процент от общего числа клеток в гемолимфе), что свидетельствует о неспособности устриц поддерживать нормальное функциональное состояние при 3% уровне насыщения воды кислородом.

https://doi.org/10.31857/S004445292201003X
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Литература

Paulmier A, Ruiz-Pino D (2009) Oxygen minimum zones (OMZs) in the modern ocean. Prog Oceanogr 80(3-4): 113-128. s://doi.org/10.1016/j.pocean.2008.08.001

Howarth R, Chan F, Conley DJ, Garnier J, Doney SC, Marino R, Billen G (2011) Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ 9(1): 18-26. s://doi.org/10.1890/100008

Sirakov I, Slavcheva-Sirakova D (2015) The influence of climate changes on the hydrobionts: a review. JBES 6(3): 315-329.

Weinstock JB, Collin R (2021) Hypoxia and warming are associated with reductions in larval bivalve abundance in a tropical lagoon. Mar Ecol Prog Ser 662: 85-95. https://doi.org/10.3354/meps13630

Wijsman JWM, Troost K, Fang J, Roncarati A (2019) Global production of marine bivalves. Trends and challenges. In Goods and services of marine bivalves (pp. 7-26). Springer, Cham.

Harris J (2008) Pacific oyster, Crassostrea gigas (Thunberg, 1793). Aquatic Invasive Species Profile Aquat Invasions: 1-12.

Gray JS, Wu RSS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment. Mar Ecol Prog Ser 238:249-279. https://doi.org/10.3354/meps238249

Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA, Bange HW, Körtzinger A (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160(8): 1875-1888. s://doi.org/10.1007/s00227-012-1954-1

Wu RS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45(1-12): 35-45. s://doi.org/10.1016/s0025-326x(02)00061-9.

Baker SM, Mann R (1992) Effects of hypoxia and anoxia on larval settlement, juvenile growth, and juvenile survival of the oyster Crassostrea virginica. Biol182(2): 265-269. https://doi.org/10.1128/AEM.00317-08

Macey B M, Achilihu IO, Burnett KG, Burnett LE (2008) Effects of hypercapnic hypoxia on inactivation and elimination of Vibrio campbellii in the Eastern oyster, Crassostrea virginica. Appl Environ Microbio 74(19): 6077-6084. s://doi.org/10.1016/j.jprot.2018.12.009

Khan B, Ringwood AH (2016) Cellular biomarker responses to hypoxia in eastern oysters and Atlantic ribbed marsh mussels. Mar Ecol Prog Ser 546: 123-133. https://doi.org/10.3354/meps11622

Sokolov EP, Markert S, Hinzke T, Hirschfeld C, Becher D, Ponsuksili S, Sokolova IM (2019) Effects of hypoxia-reoxygenation stress on mitochondrial proteome and bioenergetics of the hypoxia-tolerant marine bivalve Crassostrea gigas. J Proteom 194: 99-111. https://doi.org/10.1016/j.jprot.2018.12.009

Andreyeva AY, Gostyukhina OL, Kladchenko ES, Vodiasova EA, Chelebieva ES (2021) Acute hypoxic exposure: effect on hemocyte functional parameters and antioxidant potential in gills of the Pacific oyster, Crassostrea gigas. Mar Environ Res 105389. https://doi.org/10.1016/j.marenvres.2021.105389

Zolotarev V (1996) The Black Sea ecosystem changes related to the introduction of new mollusc species. Marine Ecology 17: 227-236. https://doi.org/10.1111/j.1439-0485.1996.tb00504.x

Allam B, Raftos D (2015) Immune responses to infectious diseases in bivalves. J Invertebr Pathol 131: 121-136. s://doi.org/10.1016/j.jip.2015.05.005

FısıER WS (1988) Environmental influence on bivalve hemocyte function. Am Fish Soc Symp 18: 225-237.

Auguste M, Balbi T, Ciacci C, Canonico B, Papa S, Borello A, Canesi L (2020) Shift in immune parameters after repeated exposure to nanoplastics in the marine bivalve Mytilus Front Immunol. 11: 426. s://doi.org/10.3389/fimmu.2020.00426

Loker ES, Adema CM, Zhang SM, Kepler TB(2004) Invertebrate immune systems–not homogeneous, not simple, not well understood. Immunol Rev 198(1): 10-24. https://doi.org/10.1111/j.0105-2896.2004.0117.x

Allam B, Espinosa EP (2016) Bivalve immunity and response to infections: are we looking at the right place? Fish Shellfish Immunol 53: 4-12. https://doi.org/10.1016/j.fsi.2016.03.037

Wootton EC, Dyrynda EA, Ratcliffe NA (2003) Bivalve immunity: comparisons between the marine mussel (Mytilus edulis), the edible cockle (Cerastoderma edule) and the razor-shell (Ensis siliqua). Fish Shellfish Immunol. 15(3): 195-210. https://doi.org/10.1016/S1050-4648(02)00161-4

Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329(5997): 1353-1355. s://doi.org/ 10.1126/science.1190689

Wang Y, Hu M, Shin PK, Cheung SG (2011) Immune responses to combined effect of hypoxia and high temperature in the green-lipped mussel Perna viridis. Mar Pollut Bull 63: 201-208 s://doi.org/10.1016/j.marpolbul.2011.05.035

Wang Y, Hu M, Cheung SG, Shin PKS, Lu W, Li J (2012) Immune parameter changes of hemocytes in green-lipped mussel Perna viridis exposure to hypoxia and hyposalinity. Aquaculture 356: 22-29. s://doi.org/10.1016/j.aquaculture.2012.06.001

Sui Y, Kong H, Shang Y, Huang X, Wu F, Hu M, Wang Y (2016) Effects of short-term hypoxia and seawater acidification on hemocyte responses of the mussel Mytilus coruscus. Mar Pollut Bull 108: 46-52. s://doi.org/10.1016/j.marpolbul.2016.05.001

Andreyeva AY, Efremova ES, Kukhareva TA (2019) Morphological and functional characterization of hemocytes in cultivated mussel (Mytilus galloprovincialis) and effect of hypoxia on hemocyte parameters. Fish Shellfish Immunol 89: 361-367.

Chen MY, Yang HS, Delaporte M, Zhao SJ, Xing K (2007) Immune responses of the scallop Chlamys farreri after air exposure to different temperatures. J Exp Mar Biol Ecol 345(1): 52-60. s://doi.org/10.1016/j.jembe.2007.01.007

Nogueira L, Mello DF, Trevisan R, Garcia D, da Silva Acosta D, Dafre AL, de Almeida EA (2017) Hypoxia effects on oxidative stress and immunocompetence biomarkers in the mussel Perna perna (Mytilidae, Bivalvia). Mar Environ Res 126: 109-115. https://doi.org/10.1016/j.marenvres.2017.02.009

Matozzo V, Monari M, Foschi J, Papi T, Cattani O, Marin MG (2005) Exposure to anoxia of the clam Chamelea gallina: I. Effects on immune responses. J Exp Mar Biol 325(2): 163-174. s://doi.org/10.1016/j.jembe.2005.04.030

Wang W, Li M, Wang L, Chen H, Liu Z, Jia Z, Song L (2017) The granulocytes are the main immunocompetent hemocytes in Crassostrea gigas. Dev Comp Immunol 67: 221-228. s://doi.org/10.1016/j.dci.2016.09.017

Piaton E, Fabre M, Goubin‐Versini I, Bretz‐Grenier MF, Courtade‐Saïdi M, Vincent S, Cochand‐Priollet B (2016) Guidelines for May‐Grünwald–Giemsa staining in haematology and non‐gynaecological cytopathology: recommendations of the French Society of Clinical Cytology (SFCC) and of the French Association for Quality Assurance in Anatomic and Cytologic Pathology (AFAQAP). Cytopathology 27(5): 359-368 https://doi.org/10.1111/cyt.12323

Kladchenko ES, Andreyeva AY, Kukhareva TA, Soldatov AA (2020). Morphologic, cytometric and functional characterisation of Anadara kagoshimensis hemocytes. Fish Shellfish Immunol 98:1030-1032.

Carballal MJ, Lopez MC, Azevedo C, Villalba A (1997) Hemolymph cell types of the mussel Mytilus galloprovincialis. Diseases of aquatic organisms 29(2):127–135.

Andreyeva AY, Kladchenko ES, Kukhareva TA, Sakhon EG (2019) Analysis of Cell Cycle and Morphological and Functional Abnormalities of Mytilus galloprovincialis Lam., 1819 (Bivalvia) Hemocytes from Coastal Ecosystems near Sevastopol, Crimea. Inland Water Biol 12(2): 96-103.

Andreyeva AY, Kladchenko ES, Vyalova OY, Kukhareva TA (2021) Functional Characterization of the Pacific Oyster, Crassostrea gigas (Bivalvia: Ostreidae), Hemocytes Under Normoxia and Short-Term Hypoxia. Turkish J Fish Aquat Sci 21(3):125-133.

Foley DA, Cheng TC (1977) Degranulation and other changes of molluscan granulocytes associated with phagocytosis. J Invertebr Pathol 29(3): 321-325. https://doi.org/10.1016/S0022-2011(77)80037-2

Rebelo MDF, Figueiredo EDS, Mariante RM, Nóbrega A, de Barros CM, Allodi S (2013) New insights from the oyster Crassostrea rhizophorae on bivalve circulating hemocytes. PLoS One 8(2): e57384. s://doi.org/10.1371/journal.pone.0057384

Lau YT, Gambino L, Santos B, Espinosa EP, Allam B (2018) Transepithelial migration of mucosal hemocytes in Crassostrea virginica and potential role in Perkinsus marinus pathogenesis. J Invertebr Pathol 153: 122-129. s://doi.org/10.1016/j.jip.2018.03.004

Ottaviani E, Franchini A, Barbieri D, Kletsas D (1998) Comparative and morphofunctional studies on Mytilus galloprovincialis hemocytes: Presence of two aging‐related hemocyte stages. Ital J Zool 65(4):349-354. s://doi.org/10.1080/11250009809386772

Delaporte M, Synard S, Pariseau J, McKenna P, Tremblay R, Davidson J, Berthe F. C (2008) Assessment of haemic neoplasia in different soft shell clam Mya arenaria populations from eastern Canada by flow cytometry. J Invertebr Pathol 98(2):190-197. https://doi.org/10.1016/j.jip.2007.12.005.

Aladaileh S, Nair SV, Birch D, Raftos DA (2007). Sydney rock oyster (Saccostrea glomerata) hemocytes: morphology and function. J Invertebr Pathol 96(1):48-63. https://doi.org/10.1016/j.jip.2007.02.011

Cima F, Matozzo V (2018) Proliferation and differentiation of circulating haemocytes of Ruditapes philippinarum as a response to bacterial challenge. Fish Shellfish Immunol 81:73-82. s://doi.org/10.1016/j.fsi.2018.07.010

de Freitas Rebelo M, de Souza Figueiredo E, Mariante RM, Nóbrega A, de Barros CM, Allodi S (2013) New insights from the oyster Crassostrea rhizophorae on bivalve circulating hemocytes. PLoS One 8(2):e57384. s://doi.org/10.1371/journal.pone.0057384

Huang J, Li S, Liu Y, Liu C, Xie L, Zhang R (2018) Hemocytes in the extrapallial space of Pinctada fucata are involved in immunity and biomineralization. Sci Rep 8(1): 1-11. https://doi.org/10.1038/s41598-018-22961-y

Michiels C, Minet E, Mottet D, Raes E (2002) Regulation of gene expression by oxygen: NF-kappaB and HIF-1, two extremes. Free Radic Biol Med 33:1231–1242. https://doi.org/10.1016/S0891-5849(02)01045-6

Donaghy L, Kraffe E, Le Goïc N, Lambert C, Volety AK, Soudant P (2012) Reactive oxygen species in unstimulated hemocytes of the Pacific oyster Crassostrea gigas: a mitochondrial involvement. PloS one 7(10): e46594. https://doi.org/10.1371/journal.pone.0046594

Donaghy L, Artigaud S, Sussarellu R, Lambert C, Le Goïc N, Hégaret H, Soudant P (2013) Tolerance of bivalve mollusc hemocytes to variable oxygen availability: a mitochondrial origin? Aquat Living Resour 26(3): 257-261. s://doi.org/10.1051/alr/2013054