Annual dynamics of North Sea bacterioplankton: seasonal variability superimposes short-term variation.

The dynamics of coastal marine microbial communities are driven by seasonally changing abiotic and biotic factors as well as by rapidly occurring short-term changes such as river fresh water influxes or phytoplankton blooms. We examined the variability of the free-living bacterioplankton at Helgoland Roads (German Bight, North Sea) over a period of one year with high temporal and taxonomic resolution to reveal variation patterns and main influencing factors. 16S rRNA gene tag sequencing of the bacterioplankton community hints at annual recurrence and resilience of few main taxa belonging to Alphaproteobacteria, Betaproteobacteria, Flavobacteriia, Acidimicrobiia and Thermoplasmata. Multiple regression analyses with various environmental factors revealed changes in water current patterns and resulting phytoplankton blooms as the main driving factors for short-term variation and temperature as the overlying factor for seasonal variation. Comparison of bacterioplankton successions during spring and summer phytoplankton blooms revealed the same dominating Flavobacteriia operational taxonomic units (OTUs) but shifts in Roseobacter related OTUs (Alphaproteobacteria) and SAR92 clade members (Gammaproteobacteria). Network analysis suggests that during spring and summer phytoplankton blooms temperature-dependent guilds are formed. In conclusion, our data imply that short-term bacterioplankton successions in response to phytoplankton blooms are indirectly affected by temperature, which is a major niche-defining factor in the German Bight.

[1]  U. Callies,et al.  Mean spring conditions at Helgoland Roads, North Sea: Graphical modeling of the influence of hydro-climatic forcing and Elbe River discharge , 2015 .

[2]  R. Amann,et al.  Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom , 2014, The ISME Journal.

[3]  A. Buchan,et al.  Master recyclers: features and functions of bacteria associated with phytoplankton blooms , 2014, Nature Reviews Microbiology.

[4]  U. Sommer,et al.  Impact of warming on phyto-bacterioplankton coupling and bacterial community composition in experimental mesocosms. , 2014, Environmental microbiology.

[5]  Christopher L. Follett,et al.  Closely related phytoplankton species produce similar suites of dissolved organic matter , 2014, Front. Microbiol..

[6]  R. Daniel,et al.  Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. , 2014, FEMS microbiology ecology.

[7]  J. Fuhrman,et al.  Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight , 2013, The ISME Journal.

[8]  Yuya Tada,et al.  Growth and distribution patterns of Roseobacter/Rhodobacter, SAR11, and Bacteroidetes lineages in the Southern Ocean , 2013, Polar Biology.

[9]  E. Ortega-Retuerta,et al.  Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie River to the Beaufort Sea (Canadian Arctic) , 2012 .

[10]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[11]  A. Wichels,et al.  Small Changes in pH Have Direct Effects on Marine Bacterial Community Composition: A Microcosm Approach , 2012, PloS one.

[12]  E. Sintes,et al.  Temporal dynamics in the free-living bacterial community composition in the coastal North Sea , 2012, FEMS microbiology ecology.

[13]  H. Sarmento,et al.  Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. , 2012, Environmental microbiology.

[14]  D. Kirchman,et al.  Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient , 2012, The ISME Journal.

[15]  U. Riebesell,et al.  Effects of rising temperature on pelagic biogeochemistry in mesocosm systems: a comparative analysis of the AQUASHIFT Kiel experiments , 2012 .

[16]  Jörg Peplies,et al.  Microbial and Chemical Characterization of Underwater Fresh Water Springs in the Dead Sea , 2012, PloS one.

[17]  R. Amann,et al.  Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom , 2012, Science.

[18]  R. Morris,et al.  Untangling Genomes from Metagenomes: Revealing an Uncultured Class of Marine Euryarchaeota , 2012, Science.

[19]  R. Knight,et al.  The Western English Channel contains a persistent microbial seed bank , 2011, The ISME Journal.

[20]  Peter Zuber,et al.  Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient , 2011, The ISME Journal.

[21]  Susan M. Huse,et al.  Defining seasonal marine microbial community dynamics , 2011, The ISME Journal.

[22]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[23]  S. Kang,et al.  Complete Genome Sequence of “Candidatus Puniceispirillum marinum” IMCC1322, a Representative of the SAR116 Clade in the Alphaproteobacteria , 2010, Journal of bacteriology.

[24]  Anders F. Andersson,et al.  Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities , 2010, The ISME Journal.

[25]  Dawn Field,et al.  The seasonal structure of microbial communities in the Western English Channel. , 2009, Environmental microbiology.

[26]  H. Ducklow,et al.  Microbial growth in the polar oceans — role of temperature and potential impact of climate change , 2009, Nature Reviews Microbiology.

[27]  R. Amann,et al.  Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. , 2009, Systematic and applied microbiology.

[28]  B. Manly,et al.  Resilience of North Sea phytoplankton spring bloom dynamics: An analysis of long‐term data at Helgoland Roads , 2008 .

[29]  U. Sommer,et al.  Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom : a mesocosm study , 2008 .

[30]  J. Gasol,et al.  Linkages between bacterioplankton community composition, heterotrophic carbon cycling and environmental conditions in a highly dynamic coastal ecosystem. , 2008, Environmental microbiology.

[31]  Stefan Schouten,et al.  Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables. , 2007, FEMS microbiology ecology.

[32]  M. Simon,et al.  Effects of phytoplankton bloom in a coastal ecosystem on the composition of bacterial communities , 2007 .

[33]  M. Pujo-Pay,et al.  Diel and Seasonal Variations in Abundance, Activity, and Community Structure of Particle-Attached and Free-Living Bacteria in NW Mediterranean Sea , 2007, Microbial Ecology.

[34]  A. Wichels,et al.  Bacterial community dynamics during the winter-spring transition in the North Sea. , 2007, FEMS microbiology ecology.

[35]  J. Gasol,et al.  Significant year‐round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system , 2007 .

[36]  E. Sintes,et al.  Abundance and activity of major groups of prokaryotic plankton in the coastal North Sea during spring and summer , 2006 .

[37]  L. Riemann,et al.  Global patterns of diversity and community structure in marine bacterioplankton , 2006, Molecular ecology.

[38]  I. Hewson,et al.  Annually reoccurring bacterial communities are predictable from ocean conditions , 2006, Proceedings of the National Academy of Sciences.

[39]  M. Cottrell,et al.  Contribution of major bacterial groups to bacterial biomass production along a salinity gradient in the South China Sea , 2006 .

[40]  M. Moran,et al.  Overview of the Marine Roseobacter Lineage , 2005, Applied and Environmental Microbiology.

[41]  R. Malmstrom,et al.  Biogeography of major bacterial groups in the Delaware Estuary , 2005 .

[42]  J. Pernthaler Predation on prokaryotes in the water column and its ecological implications , 2005, Nature Reviews Microbiology.

[43]  P. Qian,et al.  Owenweeksia hongkongensis gen. nov., sp. nov., a novel marine bacterium of the phylum 'Bacteroidetes'. , 2005, International journal of systematic and evolutionary microbiology.

[44]  J. L. Martin,et al.  Links between Phytoplankton and Bacterial Community Dynamics in a Coastal Marine Environment , 2005, Microbial Ecology.

[45]  Francesc Peters,et al.  Changes in Bacterioplankton Composition under Different Phytoplankton Regimens , 2004, Applied and Environmental Microbiology.

[46]  A. Wichels,et al.  40-year long-term study of microbial parameters near Helgoland (German Bight, North Sea): historical view and future perspectives , 2004, Helgoland Marine Research.

[47]  M. Simon,et al.  A newly discovered Roseobacter cluster in temperate and polar oceans , 2004, Nature.

[48]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[49]  Matthew T. Cottrell,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary , 2022 .

[50]  H. Grossart,et al.  Microbial ecology of organic aggregates in aquatic ecosystems , 2002 .

[51]  E. Delong,et al.  Comparison of Fluorescently Labeled Oligonucleotide and Polynucleotide Probes for the Detection of Pelagic Marine Bacteria and Archaea , 2002, Applied and Environmental Microbiology.

[52]  D. Nicolau,et al.  Two Species of Culturable Bacteria Associated With Degradation of Brown Algae Fucus Evanescens , 2002, Microbial Ecology.

[53]  R. Amann,et al.  Isolation of Novel Pelagic Bacteria from the German Bight and Their Seasonal Contributions to Surface Picoplankton , 2001, Applied and Environmental Microbiology.

[54]  W. Wiebe,et al.  Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria , 2001 .

[55]  H. Storch,et al.  Statistical Analysis in Climate Research , 2000 .

[56]  J. Baross,et al.  Characterization of the bacterially-active particle fraction in the Columbia River estuary , 2000 .

[57]  H. Ohtake,et al.  Involvement of an Extracellular Protease in Algicidal Activity of the Marine Bacterium Pseudoalteromonassp. Strain A28 , 2000, Applied and Environmental Microbiology.

[58]  T. Thingstad Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems , 2000 .

[59]  K. Šimek,et al.  Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. , 2000 .

[60]  S. Kjelleberg,et al.  Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. , 1999, FEMS microbiology ecology.

[61]  J. Hedges,et al.  Global biogeochemical cycles: progress and problems , 1992 .

[62]  Michael L. Pace,et al.  The production of dissolved organic matter by phytoplankton and its importance to bacteria : patterns across marine and freshwater systems , 1991 .

[63]  E. Sherr,et al.  High rates of consumption of bacteria by pelagic ciliates , 1987, Nature.

[64]  Barbara Mayer,et al.  Microbial Ecology Fundamentals And Applications , 2016 .

[65]  R. Amann,et al.  Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. , 2012, Environmental microbiology.

[66]  M. Simon,et al.  Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate , 2011, The ISME Journal.

[67]  S. Vázquez,et al.  Extracellular proteases from the Antarctic marine pseudoalteromonas sp. P96-47 strain. , 2008, Revista Argentina de microbiologia.

[68]  S. Giovannoni,et al.  Evolution, diversity, and molecular ecology of marine prokaryotes , 2000 .