Abstract
To ascertain the saying “Everything is everywhere, but the environment selects”, it was imperative to find out the main factor influencing bacterioplankton composition at genus level of Kongsfjorden where was influenced both by glacier melting water and Atlantic water. Thus, bacterioplankton diversity was investigated using pyrosequencing. In addition, nutrients, chlorophyll a, in situ temperature and salinity were measured. There were seventeen of 33 identified genera with relative abundance > 0.1%. Redundancy analysis showed that 73.02% of bacterioplankton community variance could be explained by environmental parameters. Furthermore, most of the abundant genera demonstrated significant correlation with environment parameters revealed by correlation analysis. Moreover, phosphate, nitrate and Chl a concentration, and the abundance of top nine identified genera varied with water mass significantly as shown by analysis of variance. Our results supported the notion that environmental factors, especially water mass had significant effect on bacterioplankton distribution at genus level. Considering the high sensitivity to environmental change and low error rate in identification, bacterioplankton at genus level could be potential bio-markers for monitoring environmental changes.
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Abbreviations
- ANOVA:
-
Analysis of variance
- Chl a :
-
Chlorophyll a
- DCA:
-
Detrended correspondence analysis
- OTUs:
-
Operational taxonomic units
- PCR:
-
Polymerase chain reaction
- PCR-DGGE:
-
Polymerase chain reaction-denaturing gel gradient electrophoresis
- pRDA:
-
Partial redundancy analysis
- RDA:
-
Redundancy analysis
- SW:
-
Surface water
- TAW:
-
Transformed atlantic water
- TIW:
-
Transformed intermediate water
References
Bowman JP, McCammon SA, Dann AL (2005) Biogeographic and quantitative analyses of abundant uncultivated γ-proteobacterial clades from marine sediment. Microb Ecol 49:451–460
Cao SN, He JF, Zhang F, Lin L, Gao Y, Zhou QM (2019) Diversity and community structure of bacterioplankton in surface waters off the northern tip of the Antarctic Peninsula. Polar Res 38:3491 https://doi.org/10.33265/polar.v38.3491
Cottier FR, Nilsen F, Inall ME, Gerland S, Tverberg V, Svendsen H (2007) Wintertime warming of an Arctic shelf in response to large-scale atmospheric circulation. Geophys Res Lett 34:L10607
Cottier FR, Tverberg V, Inall ME, Svendsen H, Nilsen F, Griffiths C (2005) Water mass modification in an Arctic fjord through cross-shelf exchange: the seasonal hydrography of Kongsfjorden Svalbard. J Geophys Res 110:C12005
De Corte D, Sintes E, Yokokawa T, Herndl GJ (2011) Changes in viral and bacterial communities during the ice-melting season in the coastal Arctic (Kongsfjorden, Ny-Alesund). Environ Microbiol 13:1827–1841
Döbler IW, Rheims H, Felske A, El-Ghezal A, Flade-Schröder D, Laatsch H, Lang S, Pukall R, Tindall BJ (2004) Oceanibulbus indolifex gen. nov., sp. nov., a North Sea alphaproteobacterium that produces bioactive metabolites. IJSEM 54:1177–1184
Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37
Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281:200–206
Fu YY, Keats KF, Rivkin RB, Lang AS (2013) Water mass and depth determine the distribution and diversity of Rhodobacterales in an Arctic marine system. FEMS Microb Ecolo 84:564–576
Genevieve LF, Belle DS, Larissa DM, Ram MM, Samir RD (2019) Prokaryotic diversity in oxygen depleted waters of the Bay of Bengal inferred using culture-dependent and -independent methods. Indian J Microbiol 59:193–199
Gerland S, Renner AHH (2007) Sea-ice mass-balance monitoring in an Arctic fjord. Ann Glaciol 46:435–442
Gosink JJ, Herwig RP, Staley JT (1997) Octadecabacter arcticus gen. nov., sp. nov., and O. antarcticus, sp. nov., nonpigmented, psychrophilic gas vacuolate bacteria from polar sea ice and water. System Appl Microbiol 20:356–365
Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis. Wiley-VCH, Weinheim, New York, Chichester, Brisbane, Singapore, Toronto
Hagen JO, Kohler J, Melvold K, Winther J (2003) Glaciers in Svalbard: mass balance, runoff and freshwater flux. Polar Res 22:145–159
Harding LW Jr, Mallonee ME, Perry ES, Miller WD, Adolf JE, Gallegos CL, Paerl HW (2016) Variable climatic conditions dominate recent phytoplankton dynamics in Chesapeake Bay. Sci Rep 6:23773
He JF, Zhang F, Lin L, Ma YX, Chen JF (2012) Bacterioplankton and picophytoplankton abundance, biomass, and distribution in the Western Canada Basin during summer 2008. Deep-sea Res Pt II 81–84:36–45
Hop H, Falk-Petersen S, Svendsen H, Kwasniewski S, Pavlov V, Pavlova O, Søreide JE (2012) Physical and biological characteristics of the pelagic system across Fram Strait to Kongsfjorden. Prog Oceanogr 71:182–231
Hunter-Cevera J, Karl D, Buckley M (2005) Marine microbial diversity: the key to earth’s habitability. American academy of microbiology, Washington DC
Hwang CY, Lee I, Cho Y, Lee YM, Jung YJ, Baek K, Nam S-II, Lee HK (2015) Sediminicola arcticus sp. nov., a psychrophilic bacterium isolated from deep-sea sediment, and emended description of the genus Sediminicola. IJSME 65:1567–1571
Ivanova EP, Zhukova NV, Lysenko AM, Gorshkova NM, Sergeev AF, Mikhailov VV, Bowman JP (2005) Loktanella agnita sp. nov. and Loktanella rosea sp. nov., from the north-west Pacific Ocean. IJSEM 55:2203–2207
Iversen RK, Seuthe L (2011) Seasonal microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): I. Heterotrophic bacteria, picoplankton and nanoflagellates. Polar Biol 34:731–749
Jain A, Krishnan KP (2017) Differences in free-living and particle-associated bacterial communities and their spatial variation in Kongsfjorden, Arctic. J Basic Microb. https://doi.org/10.1002/jobm.201700216
Jain A, Krishnan KP, Singh A, Thomas FA, Begum N, Tiwari M, Bhaskar VP, Gopinath A (2019) Biochemical composition of particles shape particle-attached bacterial community structure in a high Arctic fjord. Ecol Indic 102:581–592
Jankowska K, Wlodarska-Kowalczuk M, Wieczorek P (2005) Abundance and biomass of bacteria in two Arctic glacial fjords. Pol Polar Res 26:77–84
Ji ZQ, Gao SQ, Jin HY, He JF, Bai YC, Wang B, Yang Z, Chen JF (2014) Nutrient distribution and the influencing factors of seawater in Arctic Kongsforden, summer 2010. Acta Oceanologica Sincica 36:80–89
Jiang F, Li W, Xiao M, Dai J, Kan W, Chen L, Li W, Fang C, Peng F (2012) Luteolibacter luojiensis sp. nov., isolated from Arctic tundra soil, and emended description of the genus Luteolibacter. IJSEM 62:2259–2263
Justić D, Rabalais NN, Turner RE (1995) Stoichiometric nutrient balance and origin of coastal eutrophication. Mar Pollut Bull 30:41–46
Karner K, Obleitner F, Krismer T, Kohler J, Greuell W (2013) A decade of energy and mass balance investigations on the glacier Kongsvegen, Svalbard. J Geophys Res-Atmo 118:3986–4000
Keck A, Wiktor J, Hapter R, Nilsen R (1999) Phytoplankton assemblages related to physical gradients in an arctic, glacier-fed fjord in summer. ICES J Mar Sci 56:203–214
Khan ST, Nakagawa Y, Haryama S (2006) Sediminicola luteus gen. nov., sp. nov., a novel member of the family Flavobacteriaceae. IJSEM 56:841–845
Kirchman DL, Moran XA, Ducklow H (2009) Microbial growth in the polar oceans - role of temperature and potential impact of climate change. Nat Rev Microbiol 7:451–459
Kortsch S, Primicerio R, Beuchel F, Renaud PE, Rodrigues J, Lønne OJ, Gulliksen B (2012) Climate-driven regime shifts in Arctic marine benthos. PNAS 109:14052–14057. https://doi.org/10.1073/pnas.1207509109
Kwasniewski S, Gluchowska M, Walkusz W, Karnovsky NJ, Jakubas D, Wojczulanis-Jakubas K, Harding AMA, Goszczko I (2012) Interannual changes in zooplankton on the West Spitsbergen Shelf in relation to hydrography and their consequences for the diet of planktivorous seabirds. ICES J Mar Sci 69:890–901
Larose C, Berger S, Ferrari C, Navarro E, Dommergue A, Schneider D, Vogel TM (2010) Microbial sequences retrieved from environmental samples from seasonal arctic snow and meltwater from Svalbard, Norway. Extremophiles 14:205–212
Lefauconnier B, Vallon M, Dowdeswell J, Hagen JO, Pinglot JF, Pourchet M (1993) Global balance of Spitsbergen ice mass and prediction of its change due to climatic change. In I. Troen (ed): Symposium Global Change and Climate Change Impacts, Focusing on European Research. Copenhagen, 6–10 September 1993: EPOCH 0035 Scientific Report. European Programme on Climatology and Natural Hazards.
Lepx S, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge
Luria CM, Amaral-Zettleer LA, Ducklow HW, Rich JJ (2016) Seasonal succession of free-living bacterial communities in coastal waters of the western Antarctic Peninsula. Front Microbiol 7:1731. https://doi.org/10.3389/fmicb.2016.01731
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618
Moller AK, Barkay T, Abu Al-Soud W, Sorensen SJ, Skov H, Kroer N (2011) Diversity and characterization of mercury-resistant bacteria in snow, freshwater and sea-ice brine from the High Arctic. FEMS Microbiol Eco 75:390–401
Nedashkovskaya OI, Vancanneyt M, Kim SB, Zhukova NV, Han JH, Mikhailov VV (2009) Leeuwenhoekiella palythoae sp. nov., a new member of the family Flavobacteriaceae. IJSEM 59:3074–3077
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) Vegan: community ecology package, version. R package version 2.4.6. https://CRAN.R-project.org/package=vegan Accessed 20 May 2018
O'Sullivan LA, Rinna J, Humphreys G, Weightman AJ, Fry JC (2005) Fluviicola taffensis gen. nov., sp. nov., a novel freshwater bacterium of the family Cryomorphaceae in the phylum ‘Bacteroidetes’. IJSEM 55:2189–2194
Parsons TR (1984) A manual of chemical & biological methods for seawater analysis. Pergamon, Amsterdam
Pinhassi J, Bowman JP, Nedashkovskaya OI, Lekunberri I, Gomez-Consarnau L, Pedros-Alio C (2006) Leeuwenhoekiella blandensis sp. nov., a genome-sequenced marine member of the family Flavobacteriaceae. IJSEM 56:1489–1493
Piquet AM, Bolhuis H, Meredith MP, Buma AG (2011) Shifts in coastal Antarctic marine microbial communities during and after melt water-related surface stratification. FEMS Microbiol Eec 76:413–427
Piquet AMT, Maat DS, Confurius-Guns V, Sintes E, Herndl GJ, van de Poll WH, Wiencke C, Buma AGJ, Bolhuis H (2015) Springtime dynamics, productivity and activity of prokaryotes in two Arctic fjords. Polar Biol 39:1749–1763
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196
Qiao ZZ, Zeng YX, Dong PY, Zheng TL (2015) Bacterial community composition and abundance of planktonic bacteria in Arctic Kongsfjorden in the summer of 2011. Chin J Polar Res 27:246
Schellenberger T, Dunse T, Kääb A, Kohler J, Reijmer C (2014) Surface speed and frontal ablation of Kronebreen and Kongsbreen, NW-Svalbard, from SAR offset tracking. Cryosphere Discuss 8:6193–6233. https://doi.org/10.5194/tcd-8-6193-2014
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541
Sinha RK, Krishnan KP, Kerkar S, Divya DT (2016) Spatio-temporal monitoring and ecological significance of retrievable pelagic heterotrophic bacteria in Kongsfjorden, an Arctic Fjord. Indian J Microbiol 57:116–120
Sun FL, Wang YS, Wu ML, Jiang ZY, Sun CC, Chen H (2014) Genetic diversity of bacterial communities and gene transfer agents in northern South China Sea. PLoS ONE 9:e111892
Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, Djahanschiri B, Zeller G, Mende DR, Alberti A, Cornejo-Castillo FM, Costea PI, Cruaud C, d'Ovidio F, Engelen S, Ferrera I, Gasol JM, Guidi L, Hildebrand F, Kokoszka F, Lepoivre C, Lima-Mendez G, Poulain J, Poulos BT, Royo-Llonch M, Sarmento H, Vieira-Silva S, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Tara Oceans coordinators, Bowler C, de Vargas C, Gorsky G, Grimsley N, Hingamp P, Iudicone D, Jaillon O, Not F, Ogata H, Pesant S, Speich S, Stemmann L, Sullivan MB, Weissenbach J, Wincker P, Karsenti E, Raes J, Acinas SG, Bork P (2015) Structure and function of the global ocean microbiome. Science 348:1261359
Svendsen H, Beszcynska-Moeller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S, Ørbæk JB, Bischof K, Carlo Papucci C, Zajaczkowski M, Azzolini R, Bruland O, Wiencke C, Winther JG, Dallmann W (2002) The physical environment of Kongsfjorden-Krossfjorden, an Arctic fjord system in Svalbard. Polar Res 21:133–166
Trappen SV, Mergaert J, Swings J (2004) Loktanella salsilacus gen. nov., sp. nov., Loktanella fryxellensis sp. nov. and Loktanella vestfoldensis sp. nov., new members of the Rhodobacter group, isolated from microbial mats in Antarctic lakes. IJSEM 54:1263–1269
Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 47:327–338
Underwood GJC, Michel C, Meisterhans G, Belzile C, Witt M, Dumbrell AJ, Koch BP (2019) Organic matter from Arctic sea-ice loss alters bacterial community structure and function. Nat Clim Change. https://doi.org/10.1038/s41558-018-0391-7
Vollmers J, Voget S, Dietrich S, Gollnow K, Smits M, Meyer K, Brinkhoff T, Simon M, Daniel R (2013) Poles Apart: Arctic and Antarctic Octadecabacter strains share high genome plasticity and a new type of Xanthorhodopsin. PLoS ONE. https://doi.org/10.1371/journal.pone.0063422
Walczowski W, Piechura J, Goszczko I, Wieczorek P, Notes A (2012) Changes in Atlantic water properties: an important factor in the European Arctic marine climate. ICES J Mar Sci 69(5):864–869. https://doi.org/10.1093/icesjms/fss068
Wang GZ, Guo CY, Luo W, Cai MH, He JF (2009) The distribution of picoplankton and nanoplankton in Kongsfjorden, Svalbard during late summer 2006. Polar Bio 32:1233–1238
Wassmann P, Kosobokova KN, Slagstad D, Drinkwater KF, Hopcroft RR, Moore SE, Ellingsen I, Nelson RJ, Carmack E, Popova E, Berge J (2015) The contiguous domains of Arctic Ocean advection: trails of life and death. Prog Oceanogr 139:42–65
Winter C, Moeseneder MM, Herndl GJ, Weinbauer MG (2008) Relationship of geographic distance, depth, temperature, and viruses with prokaryotic communities in the eastern tropical Atlantic Ocean. Microbl Eco 56:383–389
Yi H, Cho JC, Chun J (2011) Pontirhabdus pectinivorans gen. nov., sp. nov., isolated from seawater. IJSEM 61:2475–2481
Yoon J, Yasumoto-Hirose M, Katsuta A, Sekiguchi H, Matsuda S, Kasai H, Yokota A (2007) Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum ‘Verrucomicrobia’ isolated from seawater in Japan. IJSEM 57:959–963. Zeng Y, Zheng T, Li H (2009) Community composition of the marine bacterioplankton in Kongsfjorden (Spitsbergen) as revealed by 16S rRNA gene analysis. Polar Bio 32:1447–1460
Zeng YX, Zhang F, He JF, Lee SH, Qiao ZY, Yu Y, Li HR (2013) Bacterioplankton community structure in the Arctic waters as revealed by pyrosequencing of 16S rRNA genes. Anton Leeuw Int J G 103:1309–1319
Zengler K (2009) Central role of the cell in microbial ecology. Microbiol Mol Biol Rev 73:712–729
Zhou LY, Wang NN, Mu DS, Liu Y, Du ZJ (2019) Coraliomargarita sinensis sp. nov., isolated from a marine solar saltern. IJSEM 69:701–707
Zhu ZY, Wu Y, Liu SM, Wenger F, Hu J, Zhang J, Zhang RF (2016) Organic carbon flux and particulate organic matter composition in Arctic valley glaciers: examples from the Bayelva River and adjacent Kongsfjorden. Biogeosciences 13:975–987. https://doi.org/10.5194/bg-13-975-2016
Acknowledgements
We give our thanks to all the members of Chinese Arctic Expedition 2012. This work was supported by the Chinese Polar Environment Comprehensive Investigation & Assessment Programs [CHNIARE-2011–2015], the National Natural Science Foundation of China [41206189 and 41476168], and Shanghai Natural Science Foundation [16ZR1439800]. Samples information and data were issued by the Resource-sharing Platform of Polar Samples (https://birds.chinare.org.cn), which was established by one of the National Science & Technology Infrastructures Polar Research Institute of China (PRIC) and Chinese National Arctic & Antarctic Data Centre (CN-NADC).
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Cao, S., Zhang, F., He, J. et al. Water masses influence bacterioplankton community structure in summer Kongsfjorden. Extremophiles 24, 107–120 (2020). https://doi.org/10.1007/s00792-019-01139-y
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DOI: https://doi.org/10.1007/s00792-019-01139-y
Keywords
- Correlation
- Bacterioplankton genus
- Environmental parameters
- Pearson
- Spearman