Cite this paper:
Tao JIANG, Xiaohan QIN, Guannan WU, Huaxian ZHAO, Xiaotao YU, Xueyan XIAO, Wenjing LIU, Qingjing HU, Jufa CHEN, Nan LI. Distribution of chromophytic phytoplankton in the Western Subarctic Gyre of Pacific Ocean revealed by morphological observation and rbcL gene sequences[J]. Journal of Oceanology and Limnology, 2023, 41(6): 2166-2179

Distribution of chromophytic phytoplankton in the Western Subarctic Gyre of Pacific Ocean revealed by morphological observation and rbcL gene sequences

Tao JIANG1, Xiaohan QIN1, Guannan WU1, Huaxian ZHAO3, Xiaotao YU2,4, Xueyan XIAO2, Wenjing LIU5, Qingjing HU2, Jufa CHEN2, Nan LI3,6
1 School of Ocean, Yantai University, Yantai 264005, China;
2 Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;
3 Key Laboratory of Ministry of Education for Environment Change and Resources Use in Beibu Gulf, Guangxi Key Laboratory of Earth Surface Processes and Intelligent Simulation, Nanning Normal University, Nanning 530001, China;
4 State Key Laboratory of Acoustics, Institute of Acoustics, Chinese Academy of Sciences, Beijing 100190, China;
5 School of Medicine, Yunnan University, Kunming 650091, China;
6 College of Ocean and Meteorology, Guangdong Ocean University, Zhanjiang 524088, China
Abstract:
Western Subarctic Gyre (WSG), which possesses distinctive differences in oceanographic and biogeochemical processes, is situated in the northwest subarctic Pacific. The WSG is characterized by high nutrient and low chlorophyll. We carried out a field investigation in this area in summer 2020 and performed microscopic observation, cytometric counting, and RuBisCO large subunit (rbcL) gene analysis to understand the community structure and spatial distribution of chromophytic phytoplankton better. Microscopic method revealed that total phytoplankton (>10 μm, including Bacillariophyta, Dinoflagellata, Ochrophyta, and Chlorophyta) abundances ranged (0.6×103)–(167.4×103) cells/L with an increasing trend from south to north. Dinoflagellates and Pennatae diatoms dominated the phytoplankton assemblages in the southern and northern stations, respectively. Major chromophytic phytoplankton groups derived from rbcL genes included Haptophyta, Ochrophyta, Bacillariophyta, as well as rarely occurring groups, such as Xanthophyta, Cyanobacteria, Dinoflagellata, Rhodophyta, and Cryptophyta. At the phylum level, Haptophyta was the most abundant phylum, accounting for approximately 30.80% of the total obtained operational taxonomic units in all samples. Ochrophyta and Bacillariophyta were the second and third most abundant phylum, and their relative abundance was 20.26% and 19.60%, respectively. Further, redundancy analysis showed that high proportion of diatoms (e.g., microscopic and rbcL methods) was positively correlated with nutrients (e.g., dissolved inorganic nitrogen (DIN), dissolved inorganic phosphorous, and dissolved silicate (DSi)) and negatively correlated with temperature and salinity. The proportion of Ochrophyta, Rhodophyta, and Cyanobateria identified by rbcL genes was positively correlated with salinity and temperature and showed negative correlation to nutrients. This work is the first molecular study of phytoplankton accomplished in the WSG, and our results show some discrepancies between morphological observation and rbcL gene sequences, which highlight the necessity of combining the microscopic and molecular methods to reveal the diversity of phytoplankton in marine environment.
Key words:    flow cytometry|microscopic counting|phytoplankton|rbcL|Western Subarctic Gyre   
Received: 2022-04-19   Revised:
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Articles by Tao JIANG
Articles by Xiaohan QIN
Articles by Guannan WU
Articles by Huaxian ZHAO
Articles by Xiaotao YU
Articles by Xueyan XIAO
Articles by Wenjing LIU
Articles by Qingjing HU
Articles by Jufa CHEN
Articles by Nan LI
References:
Aizawa C, Tanimoto M, Jordan R W.2005.Living diatom assemblages from North Pacific and Bering Sea surface waters during summer 1999.Deep Sea Research Part II:Topical Studies in Oceanography, 52(16-18):2186-2205, https://doi.org/10.1016/j.dsr2.2005.08.008.
Bolyen E, Rideout J R, Dillon M R et al.2019.Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.Nature Biotechnology, 37(8):852-857, https://doi.org/10.1038/s41587-019-0209-9.
Bradley I M, Pinto A J, Guest J S.2016.Design and evaluation of Illumina MiSeq-compatible, 18S rRNA gene-specific primers for improved characterization of mixed phototrophic communities.Applied and Environmental Microbiology, 82(19):5878-5891, https://doi.org/10.1128/AEM.01630-16.
Buck K R, Chavez F P, Campbell L.1996.Basin-wide distributions of living carbon components and the inverted trophic pyramid of the central gyre of the North Atlantic Ocean, summer 1993.Aquatic Microbial Ecology, 10(3):283-298.
Eikrem W, Romari K, Latasa M et al.2004.Florenciella parvula gen.et sp.nov.(Dictyochophyceae, Heterokontophyta), a small flagellate isolated from the English Channel.Phycologia, 43(6):658-668, https://doi.org/10.2216/i0031-8884-43-6-658.1.
Eiler A, Drakare S, Bertilsson S et al.2013.Unveiling distribution patterns of freshwater phytoplankton by a next generation sequencing based approach.PLoS One, 8(1):e53516, https://doi.org/10.1371/journal.pone.0053516.
Fujiki T, Hosoda S, Harada N.2022.Phytoplankton blooms in summer and autumn in the northwestern subarctic Pacific detected by the mooring and float systems.Journal of Oceanography, 78(2):63-72, https://doi.org/10.1007/s10872-021-00628-z.
Fujiki T, Matsumoto K, Honda M C et al.2009.Phytoplankton composition in the subarctic North Pacific during autumn 2005.Journal of Plankton Research, 31(2):179-191, https://doi.org/10.1093/plankt/fbn108.
Fujiki T, Matsumoto K, Mino Y et al.2014.Seasonal cycle of phytoplankton community structure and photophysiological state in the western subarctic gyre of the North Pacific.Limnology and Oceanography, 59(3):887-900, https://doi.org/10.4319/lo.2014.59.3.0887.
Giesbrecht K E, Varela D E, Wiktor J et al.2019.A decade of summertime measurements of phytoplankton biomass, productivity and assemblage composition in the Pacific Arctic Region from 2006 to 2016.Deep Sea Research Part II:Topical Studies in Oceanography, 162:93-113.
Harrison P J, Whitney F A, Tsuda A et al.2004.Nutrient and plankton dynamics in the NE and NW Gyres of the Subarctic Pacific Ocean.Journal of Oceanography, 60(1):93-117.
Hattori H, Koike M, Tachikawa K et al.2004.Spatial variability of living coccolithophore distribution in the western subarctic Pacific and western Bering Sea.Journal of Oceanography, 60(2):505-515, https://doi.org/10.1023/B:JOCE.0000038063.81738.ab.
Ichinomiya M, Dos Santos A L, Gourvil P et al.2016.Diversity and oceanic distribution of the Parmales (Bolidophyceae), a picoplanktonic group closely related to diatoms.The ISME Journal, 10(10):2419-2434, https://doi.org/10.1038/ismej.2016.38.
Ichinomiya M, Yoshikawa S, Kamiya M et al.2011.Isolation and characterization of Parmales (Heterokonta/Heterokontophyta/Stramenopiles) from the Oyashio region, Western North Pacific.Journal of Phycology, 47(1):144-151, https://doi.org/10.1111/j.1529-8817.2010.00926.x.
Imai K, Nojiri Y, Tsurushima N et al.2002.Time series of seasonal variation of primary productivity at station KNOT (44°N, 155°E) in the sub-arctic western North Pacific.Deep Sea Research Part II:Topical Studies in Oceanography, 49(24-25):5395-5408.
Jiang T, Chai C, Wang J F et al.2016.Temporal and spatial variations of abundance of phycocyanin- and phycoerythrin-rich Synechococcus in Pearl River Estuary and adjacent coastal area.Journal of Ocean University of China, 15(5):897-904, https://doi.org/10.1007/s11802-016-3011-z.
John D E, Patterson S S, Paul J H.2007.Phytoplankton-group specific quantitative polymerase chain reaction assays for RuBisCO mRNA transcripts in seawater.Marine Biotechnology, 9(6):747-759, https://doi.org/10.1007/s10126-007-9027-z.
Karlson B, Andersen P, Arneborg L et al.2021.Harmful algal blooms and their effects in coastal seas of northern Europe.Harmful Algae, 102:101989, https://doi.org/10.1016/j.hal.2021.101989.
Komuro C, Narita H, Imai K et al.2005.Microplankton assemblages at Station KNOT in the subarctic western Pacific, 1999-2000.Deep Sea Research Part II:Topical Studies in Oceanography, 52(16-18):2206-2217, https://doi.org/10.1016/j.dsr2.2005.08.006.
Kwak J H, Lee S H, Hwang J et al.2014.Summer primary productivity and phytoplankton community composition driven by different hydrographic structures in the East/Japan Sea and the Western Subarctic Pacific.Journal of Geophysical Research:Oceans, 119(7):4505-4519, https://doi.org/10.1002/2014jc009874.
Li B L, Karl D M, Letelier R M et al.2013.Variability of chromophytic phytoplankton in the North Pacific Subtropical Gyre.Deep Sea Research Part II:Topical Studies in Oceanography, 93:84-95, https://doi.org/10.1016/j.dsr2.2013.03.007.
Li N, Yu S X, Wang Y C et al.2016.Diversity of phototrophic phytoplankton in Northern South China Sea indicated by rbcL analysis.Journal of Applied Phycology, 28(2):773-781, https://doi.org/10.1007/s10811-015-0624-3.
Liu H, Probert I, Uitz J et al.2009.Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans.Proceedings of the National Academy of Sciences of the United States of America, 106(31):12803-12808, https://doi.org/10.1073/pnas.0905841106.
Liu H B, Imai K, Suzuki K et al.2002a.Seasonal variability of picophytoplankton and bacteria in the western subarctic Pacific Ocean at station KNOT.Deep Sea Research Part II:Topical Studies in Oceanography, 49(24-25):5409-5420, https://doi.org/10.1016/S0967-0645 (02)00199-6.
Liu H B, Suzuki K, Minami C et al.2002b.Picoplankton community structure in the subarctic Pacific Ocean and the Bering Sea during summer 1999.Marine Ecology Progress Series, 237:1-14, https://doi.org/10.3354/meps 237001.
Liu H B, Suzuki K, Saito H.2004.Community structure and dynamics of phytoplankton in the western subarctic Pacific Ocean:a synthesis.Journal of Oceanography, 60(1):119-137, https://doi.org/10.1023/B:JOCE.0000038322.79644.36.
Liu Y J, Yang G P, Guan X J et al.2006.Genetic diversity and its seasonal variation of jiaozhou bay phytoplankton determined by rbcL gene sequencing.Acta Oceanologica Sinica, 25(2):125-134.
Mackenzie L A, Smith K F, Rhodes L L et al.2011.Mortalities of sea-cage salmon (Oncorhynchus tshawytscha) due to a bloom of Pseudochattonella verruculosa (Dictyochophyceae) in Queen Charlotte Sound, New Zealand.Harmful Algae, 11:45-53, https://doi.org/10.1016/j.hal.2011.07.003.
Mardones J I, Fuenzalida G, Zenteno K et al.2019.Salinity-growth response and ichthyotoxic potency of the Chilean Pseudochattonella verruculosa.Frontiers in Marine Science, 6:24, https://doi.org/10.3389/fmars.2019.00024.
Matsumoto K, Honda M C, Sasaoka K et al.2014.Seasonal variability of primary production and phytoplankton biomass in the western pacific subarctic gyre:control by light availability within the mixed layer.Journal of Geophysical Research:Oceans, 119(9):6523-6534, https://doi.org/10.1002/2014JC009982.
Mochizuki M, Shiga N, Saito M et al.2002.Seasonal changes in nutrients, chlorophyll a and the phytoplankton assemblage of the western subarctic gyre in the Pacific Ocean.Deep Sea Research Part II:Topical Studies in Oceanography, 49(24-25):5421-5439, https://doi.org/10.1016/S0967-0645(02)00209-6.
Morse D, Salois P, Markovic P et al.1995.A nuclear-encoded form II RuBisCO in dinoflagellates.Science, 268(5217):1622-1624, https://doi.org/10.1126/science.7777861.
Nishioka J, Hirawake T, Nomura D et al.2021.Iron and nutrient dynamics along the East Kamchatka Current, western Bering Sea Basin and Gulf of Anadyr.Progress in Oceanography, 198:102662, https://doi.org/10.1016/j.pocean.2021.102662.
Nishioka J, Obata H, Ogawa H et al.2020.Sub-polar marginal seas fuel the North Pacific through the intermediate water at the termination of the global ocean circulation.Proceedings of the National Academy of Sciences of the United States of America, 117(23):12665-12673, https://doi.org/10.1073/pnas.2000658117.
Nishioka J, Ono T, Saito H et al.2011.Oceanic iron supply mechanisms which support the spring diatom bloom in the Oyashio region, western subarctic Pacific.Journal of Geophysical Research:Oceans, 116(C2):C02021.
Nishioka J, Takeda S, Kudo I et al.2003.Size-fractionated iron distributions and iron-limitation processes in the subarctic NW Pacific.Geophysical Research Letters, 30(14):1730, https://doi.org/10.1029/2002GL016853.
Obayashi Y, Tanoue E, Suzuki K et al.2001.Spatial and temporal variabilities of phytoplankton community structure in the northern North Pacific as determined by phytoplankton pigments.Deep Sea Research Part I:Oceanographic Research Papers, 48(2):439-469, https://doi.org/10.1016/S0967-0637(00)00036-4.
Park M G, Kim S, Kim H S et al.2006.First successful culture of the marine dinoflagellate Dinophysis acuminata.Aquatic Microbial Ecology, 45(2):101-106, https://doi.org/10.3354/ame045101.
Pujari L, Narale D, Kan J J et al.2021.Distribution of chromophytic phytoplankton in the eddy-induced upwelling region of the west Pacific Ocean revealed using rbcL genes.Frontiers in Microbiology, 12:596015, https://doi.org/10.3389/fmicb.2021.596015.
Pujari L, Wu C, Kan J J et al.2019.Diversity and spatial distribution of chromophytic phytoplankton in the Bay of Bengal revealed by RuBisCO genes (rbcL).Frontiers in Microbiology, 10:1501, https://doi.org/10.3389/fmicb.2019.01501.
Rii Y M, Bidigare R R, Church M J.2018.Differential responses of eukaryotic phytoplankton to nitrogenous nutrients in the North Pacific Subtropical Gyre.Frontiers in Marine Science, 5:92, https://doi.org/10.3389/fmars.2018.00092.
Roden G I.1991.Subarctic-subtropical transition zone of the North Pacific:large-scale aspects and mesoscale structure.NOAA Technical Report NMFS, 105(1):1-38, https://doi.org/10.5194/bg-5-353-2008.
Rognes T, Flouri T, Nichols B et al.2016.VSEARCH:a versatile open source tool for metagenomics.PeerJ, 4:e2584, https://doi.org/10.7717/peerj.2584.
Samanta B, Bhadury P.2014.Analysis of diversity of chromophytic phytoplankton in a mangrove ecosystem using rbcL gene sequencing.Journal of Phycology, 50(2):328-340, https://doi.org/10.1111/jpy.12163.
Samanta B, Bhadury P.2016.A comprehensive framework for functional diversity patterns of marine chromophytic phytoplankton using rbcL phylogeny.Scientific Reports, 6(1):20783, https://doi.org/10.1038/srep20783.
Sarthou G, Timmermans K R, Blain S et al.2005.Growth physiology and fate of diatoms in the ocean:a review.Journal of Sea Research, 53(1-2):25-42, https://doi.org/10.1016/j.seares.2004.01.007.
Strickland J D H, Parsons T R.1972.A Practical Handbook of Seawater Analysis.Fisheries Research Board of Canada, Ottawa.310p.
Suzuki K, Minami C, Liu H B et al.2002.Temporal and spatial patterns of chemotaxonomic algal pigments in the subarctic Pacific and the Bering Sea during the early summer of 1999.Deep Sea Research Part II:Topical Studies in Oceanography, 49(24-25):5685-5704, https://doi.org/10.1016/S0967-0645(02)00218-7.
Taylor F J R, Waters R E.1982.Spring phytoplankton in the subarctic North Pacific Ocean.Marine Biology, 67(3):323-335, https://doi.org/10.1007/BF00397673.
Tsurushima N, Nojiri Y, Imai K et al.2002.Seasonal variations of carbon dioxide system and nutrients in the surface mixed layer at station KNOT (44°N, 155°E) in the subarctic western North Pacific.Deep Sea Research Part II:Topical Studies in Oceanography, 49(24-25):5377-5394, https://doi.org/10.1016/S0967-0645(02)00197-2.
Uitz J, Claustre H, Gentili B et al.2010.Phytoplankton class-specific primary production in the world's oceans:seasonal and Interannual variability from satellite observations.Global Biogeochemical Cycles, 24(3):GB3016, https://doi.org/10.1029/2009gb003680.
Utermöhl H.1958.Methods of collecting plankton for various purposes are discussed.SIL Communications, 1953-1996, 9(1):1-38, https://doi.org/10.1080/05384680.1958.11904091
Waga H, Fujiwara A, Hirawake T et al.2022.Primary productivity and phytoplankton community structure in surface waters of the western subarctic Pacific and the Bering Sea during summer with reference to bloom stages.Progress in Oceanography, 201:102738, https://doi.org/10.1016/j.pocean.2021.102738.
Xu H H, Tabita F R.1996.Ribulose-1, 5-bisphosphate carboxylase/oxygenase gene expression and diversity of Lake Erie planktonic microorganisms.Applied and Environmental Microbiology, 62(6):1913-1921, https://doi.org/10.1128/aem.62.6.1913-1921.1996.
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