Cite this paper:
Ting WANG, Xi CHEN, Jialin LI, Song QIN. Distribution and phenogenetic diversity of Synechococcus in the Bohai Sea, China[J]. Journal of Oceanology and Limnology, 2022, 40(2): 592-604

Distribution and phenogenetic diversity of Synechococcus in the Bohai Sea, China

Ting WANG1,2, Xi CHEN3, Jialin LI2,4, Song QIN2,4
1 College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China;
2 Key Lab of Coastal Biology and Biological Resource Utilization, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, China;
3 College of Marine Life Science, Ocean University of China, Qingdao 266005, China;
4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
Abstract:
Synechococcus is one of the most abundant picocyanobacteria in marine ecosystem, and the absence of Prochlorococcus would make it indispensable as a primary producer in the Bohai Sea, North China. However, the abundance distribution and genetic diversity of Synechococcus in this region have rarely been reported. In this study, the distribution pattern of Synechococcus abundance was investigated during four cruises in April, June, August, and November from 2018 to 2019, moreover, its phenogenetic diversity was studied based on high-throughput sequencing of the cpeBA operon. The results demonstrate that phycoerythrin-containing Synechococcus was most abundant in August when temperature was high and oxygen saturation was low. During this period, Synechococcus pigment type (PT) 2 was abundant in the Bohai Bay and Laizhou Bay under conditions of high nutrient concentration, temperature, and turbidity. In comparison, PT3, especially those clusters characterized with high or variable ratio of phycourobilin and phycoerythrobilin, was predominant in the Bohai Strait and Liaodong Bay under conditions of high salinity, pH, and oxygen saturation. Furthermore, co-occurrence correlations using network analysis revealed that Synechococcus PTs were related to 15.37%-43.48% of the prokaryotic genera. Synechococcus PT3c/PT3d and PT2 were the most important PTs in the network. The hierarchical clustering revealed that taxa cooccurred with Synechococcus PTs differed among samples. It could be attributed to the substance exchange and the environmental impact, which calls for more studies in the future.
Key words:    Synechococcus|phenogenetic diversity|co-occurrence network|coastal ecosystem|Bohai Sea   
Received: 2021-01-05   Revised:
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References:
Bastian M, Heymann S, Jacomy M.2009.Gephi:an open source software for exploring and manipulating networks.In:International AAAI Conference on weblogs and social media:San Jose, California, https://gephi.org/publications/gephi-bastian-feb09.pdf.
Bertilsson S, Berglund O, Karl D M, Chisholm S W.2003.Elemental composition of marine Prochlorococcus and Synechococcus:implications for the ecological stoichiometry of the sea.Limnology and Oceanography, 48(5):1721-1731.
Bokulich N A, Subramanian S, Faith J J, Gevers D, Gordon J I, Knight R, Mills D A, Caporaso J G.2013.Qualityfiltering vastly improves diversity estimates from Illumina amplicon sequencing.Nature Methods, 10(1):57-59.
Brown J, Pirrung M, McCue L A.2017.FQC Dashboard:integrates FastQC results into a web-based, interactive, and extensible FASTQ quality control tool.Bioinformatics, 33(19):3137-3139.
Chen F, Wang K, Kan J J, Bachoon D S, Lu J R, Lau S, Campbell L.2004.Phylogenetic diversity of Synechococcus in the Chesapeake Bay revealed by Ribulose-1,5-bisphosphate carboxylase-oxygenase(RuBisCO) large subunit gene (rbcL) sequences.Aquatic Microbial Ecology, 36(2):153-164.
Chin C H, Chen S H, Wu H H, Ho C W, Ko M T, Lin C Y.2014.cytoHubba:identifying hub objects and sub-networks from complex interactome.BMC Systems Biology, 8(4):S11.
Christie-Oleza J A, Scanlan D J, Armengaud J.2015."You produce while I clean up", a strategy revealed by exoproteomics during Synechococcus-Roseobacter interactions.Proteomics, 15(20):3454-3462.
Christie-Oleza J A, Sousoni D, Lloyd M, Armengaud J, Scanlan D J.2017.Nutrient recycling facilitates longterm stability of marine microbial phototroph-heterotroph interactions.Nature Microbiology, 2(9):17100.
Chung C C, Gong G C, Huang C Y, Lin J Y, Lin Y C.2015.Changes in the Synechococcus assemblage composition at the surface of the East China Sea due to flooding of the Changjiang River.Microbial Ecology, 70(3):677-688.
Cuevas L A, Morales C E.2006.Nanoheterotroph grazing on bacteria and cyanobacteria in oxic and suboxic waters in coastal upwelling areas off northern Chile.Journal of Plankton Research, 28(4):385-397.
Dafner E V.2015.Segmented continuous-flow analyses of nutrient in seawater:intralaboratory comparison of Technicon AutoAnalyzer II and Bran+ Luebbe Continuous Flow AutoAnalyzer III.Limnology and Oceanography:Methods, 13(10):511-520.
del Carmen Muñoz-Marín M, Gómez-Baena G, Díez J, Beynon R J, González-Ballester D, Zubkov M V, GarcíaFernández J M.2017.Glucose uptake in Prochlorococcus:diversity of kinetics and effects on the metabolism.Frontiers in Microbiology, 8:327.
Dvořák P, Casamatta D A, Poulíčková A, Hašler P, Ondřej V, Sanges R.2014.Synechococcus:3 billion years of global dominance.Molecular Ecology, 23(22):5538-5551.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R.2011.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics, 27(16):2194-2200.
Everroad R C, Wood A M.2006.Comparative molecular evolution of newly discovered picocyanobacterial strains reveals a phylogenetically informative variable region of β-phycoerythrin.Journal of Phycology, 42(6):1300-1311.
Everroad R C, Wood A M.2012.Phycoerythrin evolution and diversification of spectral phenotype in marine Synechococcus and related picocyanobacteria.Molecular Phylogenetics and Evolution, 64(3):381-392.
Flombaum P, Gallegos J L, Gordillo R A, Rincón J, Zabala L L, Jiao N Z, Karl D M, Li W K W, Lomas M W, Veneziano D, Vera C S, Vrugt J A, Martiny A C.2013.Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus.Proceedings of the National Academy of Sciences of the United States of America, 110(24):9824-9829.
Fox J, Weisberg S.2019.An R Companion to Applied Regression.3rd edn.SAGE Publications, Thousand Oaks, CA, USA.Grébert T, Doré H, Partensky F, Farrant G K, Boss E S, Picheral M, Guidi L, Pesant S, Scanlan D J, Wincker P, Acinas S G, Kehoe D M, Garczarek L.2018.Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria.Proceedings of the National Academy of Sciences of the United States of America, 115(9):E2010-E2019.
Guidi L, Chaffron S, Bittner L, Eveillard D, Larhlimi A, Roux S, Darzi Y, Audic S, Berline L, Brum J R, Coelho L P, Espinoza J C I, Malviya S, Sunagawa S, Dimier C, Kandels-Lewis S, Picheral M, Poulain J, Searson S, Coordinators T O C, Stemmann L, Not F, Hingamp P, Speich S, Follows M, Karp-Boss L, Boss E, Ogata H, Pesant S, Weissenbach J, Wincker P, Acinas S G, Bork P, de Vargas C, Iudicone D, Sullivan M B, Raes J, Karsenti E, Bowler C, Gorsky G.2016.Plankton networks driving carbon export in the oligotrophic ocean.Nature, 532(7600):465-470.
Haaber J, Middelboe M.2009.Viral lysis of Phaeocystis pouchetii:implications for algal population dynamics and heterotrophic C, N and P cycling.The ISME Journal, 3(4):430-441.
Haverkamp T H A, Schouten D, Doeleman M, Wollenzien U, Huisman J, Stal L J.2009.Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the Baltic Sea.The ISME Journal, 3(4):397-408.
Herdman H, Castenholz R W, Waterbury J B, Rippka R.2001.Form-genus XIII.Synechococcus.In:Boone D R and Castenholz R W ed.Bergey's Manual of Systematic Bacteriology.Springer, Dordrecht.p.508-512.
Hunter-Cevera K R, Post A F, Peacock E E, Sosik H M.2016.Diversity of Synechococcus at the Martha's Vineyard coastal observatory:insights from culture isolations, clone libraries, and flow cytometry.Microbial Ecology, 71(2):276-289.
Ihaka R, Gentleman R.1996.R:a language for data analysis and graphics.Journal of Computational and Graphical Statistics, 5(3):299-314.
Johnson Z I, Zinser E R, Coe A, Mcnulty N P, Woodward E M S, Chisholm S W.2006.Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients.Science, 311(5768):1737-1740.
Kent A G, Baer S E, Mouginot C, Huang J S, Larkin A A, Lomas M W, Martiny A C.2019.Parallel phylogeography of Prochlorococcus and Synechococcus.The ISME Journal, 13(2):430-441.
Kumar S, Tamura K, Nei M.1994.MEGA:molecular evolutionary genetics analysis software for microcomputers.Bioinformatics, 10(2):189-191.
Larsson J, Celepli N, Ininbergs K, Dupont C L, Yooseph S, Bergman B, Ekman M.2014.Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea.The ISME Journal, 8(9):1892-1903.
Letunic I, Bork P.2019.Interactive Tree Of Life (iTOL) v4:recent updates and new developments.Nucleic Acids Research, 47(W1):W256-W259.
Li H B, Xiao T, Ding T, Lü R H.2006.Effect of the Yellow Sea Cold Water Mass (YSCWM) on distribution of bacterioplankton.Acta Ecologica Sinica, 26(4):1012-1019.
Li J J, Chen Z Z, Jing Z Y, Zhou L B, Li G, Ke Z X, Jiang X, Liu J X, Liu H X, Tan Y H.2019a.Synechococcus bloom in the Pearl River Estuary and adjacent coastal area-with special focus on flooding during wet seasons.Science of the Total Environment, 692:769-783.
Li J L, Wang T, Yu S X, Bai J, Qin S.2019b.Community characteristics and ecological roles of bacterial biofilms associated with various algal settlements on coastal reefs.Journal of Environmental Management, 250:109459.
Li W K W.1998.Annual average abundance of heterotrophic bacteria and Synechococcus in surface ocean waters.
Limnology and Oceanography, 43(7):1746-1753.
Louca S, Parfrey L W, Doebeli M.2016.Decoupling function and taxonomy in the global ocean microbiome.Science, 353(6305):1272-1277.
Lü D W, Zheng B, Fang Y, Shen G, Liu H J.2015.Distribution and pollution assessment of trace metals in seawater and sediment in Laizhou Bay.Chinese Journal of Oceanology and Limnology, 33(4):1053-1061.
Martiny A C, Treseder K, Pusch G.2013.Phylogenetic conservatism of functional traits in microorganisms.The ISME Journal, 7(4):830-838.
McCarren J, Becker J W, Repeta D J, Shi Y M, Young C R, Malmstrom R R, Chisholm S W, DeLong E F.2010.
Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea.Proceedings of the National Academy of Sciences of the United States of America, 107(38):16420-16427.
Middelboe M, Riemann L, Steward G F, Hansen V, Nybroe O.2003.Virus-induced transfer of organic carbon between marine bacteria in a model community.Aquatic Microbial Ecology, 33(1):1-10.
Moore L R, Post A F, Rocap G, Chisholm S W.2002.Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus.Limnology and Oceanography, 47(4):989-996.
Oksanen J, Blanchet F G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara R B, Simpson GL, Solymos P, Stevens M H H, Szoecs E, Wagner H.2019.Vegan:communityecology package project, https://CRAN.R-project.org/package=vegan Olson R J, Chisholm S W, Zettler E R, Armbrust E V.1988.Analysis of Synechococcus pigment types in the sea using single and dual beam flow cytometry.Deep Sea Research Part A.Oceanographic Research Papers, 35(3):425-440.
Paerl H W.1991.Ecophysiological and trophic implications of light-stimulated amino acid utilization in marine picoplankton.Applied and Environmental Microbiology, 57(2):473-479.
Partensky F, Blanchot J, Vaulot D.1999.Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters:a review.Bulletin de l'Institut Océanographique (Monaco), 19:457-476.
Ruiz-González C, Simó R, Vila-Costa M, Sommaruga R, Gasol J M.2012.Sunlight modulates the relative importance of heterotrophic bacteria and picophytoplankton in DMSPsulphur uptake.The ISME Journal, 6(3):650-659.
Saito M A, Moffett J W, Chisholm S W, Waterbury J B.2002.Cobalt limitation and uptake in Prochlorococcus.Limnology and Oceanography, 47(6):1629-1636.
Saito M A, Rocap G, Moffett J W.2005.Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome.Limnology and Oceanography, 50(1):279-290.
Scanlan D J.2012.Marine picocyanobacteria.In:Whitton B A ed.Ecology of Cyanobacteria II.Springer, Dordrecht.p.503-533.
Schlitzer R.2002.Interactive analysis and visualization of geoscience data with Ocean Data View.Computers & Geosciences, 28(10):1211-1218.
Tai V, Paulsen I T, Phillippy K, Johnson D A, Palenik B.2009.Whole-genome microarray analyses of SynechococcusVibrio interactions.Environmental Microbiology, 11(10):2698-2709.
Talmy D, Beckett S J, Zhang A B, Taniguchi D A A, Weitz J S, Follows M J.2019.Contrasting controls on microzooplankton grazing and viral infection of microbial prey.Frontiers in Marine Science, 6:182.
van den Engh G J, Doggett J K, Thompson A W, Doblin M A, Gimpel C N G, Karl D M.2017.Dynamics of Prochlorococcus and Synechococcus at station ALOHA revealed through flow cytometry and high-resolution vertical sampling.Frontiers in Marine Science, 4:359.
Walters W, Hyde E R, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, Gilbert J A, Jansson J K, Caporaso J G, Fuhrman J A, Apprill A, Knight R.2016.Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys.mSystems, 1(1):e00009-15.
Wei H, Sun J, Moll A, Zhao L.2004.Phytoplankton dynamics in the Bohai Sea-observations and modelling.Journal of Marine Systems, 44(3-4):233-251.
Wood A M, Phinney D A, Yentsch C S.1998.Water column transparency and the distribution of spectrally distinct forms of phycoerythrin-containing organisms.Marine Ecology Progress Series, 162:25-31.
Xia X M, Liu H B, Choi D, Noh J H.2018.Variation of Synechococcus pigment genetic diversity along two turbidity gradients in the China Seas.Microbial Ecology, 75(1):10-21.
Yan G W, Jiang T, Zhang Y Y, Cui Z G, Qu K M, Zheng Y Y, Lu L, Li Y.2020.Determining temporal and spatial distribution of autotrophic picoplankton community composition through HPLC-pigment method and flow cytometry in the central Bohai Sea (China).Marine Pollution Bulletin, 157:111261.
Zhang G G, Huang J, Jia M Q, Liu F H, Yang Y H, Wang Z W, Han G D.2019.Ammonia-oxidizing bacteria and archaea:response to simulated climate warming and nitrogen supplementation.Soil Science Society of America Journal, 83(6):1683-1695.
Zhang Y, Lu X Q, Liu H L, Liu Q Q, Yu D.2015.Identifying the sources of organic matter in marine and riverine sediments of Bohai Bay and its catchment using carbon and nitrogen stable isotopes.Chinese Journal of Oceanology and Limnology, 33(1):204-209.
Zhao Y, Yu R C, Kong F Z, Wei C J, Liu Z, Geng H X, Dai L, Zhou Z X, Zhang Q C, Zhou M J.2019.Distribution patterns of picosized and nanosized phytoplankton assemblages in the East China Sea and the Yellow Sea:implications on the impacts of kuroshio intrusion.Journal of Geophysical Research:Oceans, 124(2):1262-1276.
Zhao Y, Zhao L, Xiao T, Liu C G, Sun J, Zhou F, Liu S M, Huang L F.2013.Temporal variation of picoplankton in the spring bloom of Yellow Sea, China.Deep Sea Research Part II:Topical Studies in Oceanography, 97:72-84.
Zhao Y, Zhao L, Zhang W C, Sun J, Huang L F, Li J, Zhai H C, Liu S M, Xiao T.2016.Variations of picoplankton abundances during blooms in the East China Sea.Deep Sea Research Part II:Topical Studies in Oceanography, 124:100-108.
Zheng Q, Lin W X, Wang Y, Li Y Y, He C, Shen Y, Guo W D, Shi Q, Jiao N Z.2021.Highly enriched N-containing organic molecules of Synechococcus lysates and their rapid transformation by heterotrophic bacteria.Limnology and Oceanography, 66(2):335-348.
Zheng Q, Wang Y, Lu J Y, Lin W X, Chen F, Jiao N Z.2020.Metagenomic and metaproteomic insights into photoautotrophic and heterotrophic interactions in a Synechococcus culture.mBio, 11(1):e03261-19.
Zheng Q, Wang Y, Xie R, Lang A S, Liu Y T, Lu J Y, Zhang X D, Sun J, Suttle C A, Jiao N Z.2018.Dynamics of heterotrophic bacterial assemblages within Synechococcus cultures.Applied and Environmental Microbiology, 84(3):e01517-17.
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