Winners and Losers of Atlantification: The Degree of Ocean Warming Affects the Structure of Arctic Microbial Communities

Arctic microbial communities (i.e., protists and bacteria) are increasingly subjected to an intrusion of new species via Atlantification and an uncertain degree of ocean warming. As species differ in adaptive traits, these oceanic conditions may lead to compositional changes with functional implications for the ecosystem. In June 2021, we incubated water from the western Fram Strait at three temperatures (2 °C, 6 °C, and 9 °C), mimicking the current and potential future properties of the Arctic Ocean. Our results show that increasing the temperature to 6 °C only minorly affects the community, while an increase to 9 °C significantly lowers the diversity and shifts the composition. A higher relative abundance of large hetero- and mixotrophic protists was observed at 2 °C and 6 °C compared to a higher abundance of intermediate-sized temperate diatoms at 9 °C. The compositional differences at 9 °C led to a higher chlorophyll a:POC ratio, but the C:N ratio remained similar. Our results contradict the common assumption that smaller organisms and heterotrophs are favored under warming and strongly indicate a thermal limit between 6 °C and 9 °C for many Arctic species. Consequently, the magnitude of temperature increase is a crucial factor for microbial community reorganization and the ensuing ecological consequences in the future Arctic Ocean.

[1]  M. Babin,et al.  Interactive effects of temperature and nitrogen source on the elemental stoichiometry of a polar diatom , 2022, Limnology and Oceanography.

[2]  T. Vihma,et al.  The Arctic has warmed nearly four times faster than the globe since 1979 , 2022, Communications Earth & Environment.

[3]  Hans C. Bernstein,et al.  Diversity and Selection of Surface Marine Microbiomes in the Atlantic-Influenced Arctic , 2022, Frontiers in Microbiology.

[4]  T. Rynearson,et al.  Thermal trait variation may buffer Southern Ocean phytoplankton from anthropogenic warming , 2022, Global change biology.

[5]  C. Bienhold,et al.  Variations of microbial communities and substrate regimes in the eastern Fram Strait between summer and fall. , 2022, Environmental microbiology.

[6]  Chang Jae Choi,et al.  Phytoplankton Surveys in the Arctic Fram Strait Demonstrate the Tiny Eukaryotic Alga Micromonas and Other Picoprasinophytes Contribute to Deep Sea Export , 2022, Microorganisms.

[7]  Bingzhang Chen Thermal diversity affects community responses to warming , 2022, Ecological Modelling.

[8]  D. Vaulot,et al.  Diversity and biogeography of planktonic diatoms in Svalbard fjords: The role of dispersal and Arctic endemism in phytoplankton community structuring , 2022, Elementa: Science of the Anthropocene.

[9]  H. Hillebrand,et al.  Cell size as driver and sentinel of phytoplankton community structure and functioning , 2021, Functional Ecology.

[10]  P. Buttigieg,et al.  Microbial diversity through an oceanographic lens: refining the concept of ocean provinces through trophic-level analysis and productivity-specific length scales. , 2021, Environmental microbiology.

[11]  A. D. Barton,et al.  Marine phytoplankton functional types exhibit diverse responses to thermal change , 2021, Nature Communications.

[12]  J. Chiggiato,et al.  Rapid Atlantification along the Fram Strait at the beginning of the 20th century , 2021, Science advances.

[13]  N. Zimmermann,et al.  Major restructuring of marine plankton assemblages under global warming , 2021, Nature Communications.

[14]  T. L. Rasmussen,et al.  Decadal trend of plankton community change and habitat shoaling in the Arctic gateway recorded by planktonic foraminifera , 2021, bioRxiv.

[15]  P. Kaiser,et al.  Effects of a Submesoscale Oceanographic Filament on Zooplankton Dynamics in the Arctic Marginal Ice Zone , 2021, Frontiers in Marine Science.

[16]  Michael Greenacre,et al.  Compositional Data Analysis , 2021, Annual Review of Statistics and Its Application.

[17]  E. Marañón,et al.  Effect of temperature on the unimodal size scaling of phytoplankton growth , 2021, Scientific reports.

[18]  Karen L. Smith,et al.  Arctic amplification of climate change: a review of underlying mechanisms , 2021 .

[19]  M. Schartau,et al.  Spatio-Temporal Variations in Community Size Structure of Arctic Protist Plankton in the Fram Strait , 2021, Frontiers in Marine Science.

[20]  F. Not,et al.  A dataset on trophic modes of aquatic protists , 2020, Biodiversity data journal.

[21]  S. Kelley,et al.  An application of compositional data analysis to multiomic time-series data , 2020, NAR genomics and bioinformatics.

[22]  I. Obernosterer,et al.  Seasonal dynamics of prokaryotes and their associations with diatoms in the Southern Ocean as revealed by an autonomous sampler. , 2020, Environmental microbiology.

[23]  P. Karlovsky,et al.  Improved normalization of species count data in ecology by scaling with ranked subsampling (SRS): application to microbial communities , 2020, PeerJ.

[24]  A. Dabrowska,et al.  Spatial Patterns of Particles and Plankton in the Warming Arctic Fjord (Isfjorden, West Spitsbergen) in Seven Consecutive Mid-Summers (2013–2019) , 2020, Frontiers in Marine Science.

[25]  A. Boetius,et al.  Summertime Chlorophyll a and Particulate Organic Carbon Standing Stocks in Surface Waters of the Fram Strait and the Arctic Ocean (1991–2015) , 2020, Frontiers in Marine Science.

[26]  C. Schaum,et al.  Functional redundancy in natural pico-phytoplankton communities depends on temperature and biogeography , 2020, bioRxiv.

[27]  L. Oziel,et al.  Faster Atlantic currents drive poleward expansion of temperate phytoplankton in the Arctic Ocean , 2020, Nature Communications.

[28]  T. Rynearson,et al.  Variability approaching the thermal limits can drive diatom community dynamics , 2020, Limnology and Oceanography.

[29]  G. Yvon‐Durocher,et al.  Abrupt declines in marine phytoplankton production driven by warming and biodiversity loss in a microcosm experiment , 2020, Ecology letters.

[30]  A. Irwin,et al.  Capacity of the common Arctic picoeukaryote Micromonas to adapt to a warming ocean , 2019, Limnology and Oceanography Letters.

[31]  K. Matsumoto,et al.  A meta-analysis on environmental drivers of marine phytoplankton C : N : P , 2019, Biogeosciences.

[32]  J. Gibert Temperature directly and indirectly influences food web structure , 2019, Scientific Reports.

[33]  G. Underwood,et al.  Organic matter from Arctic sea-ice loss alters bacterial community structure and function , 2019, Nature Climate Change.

[34]  Hongbin Liu,et al.  Marine phytoplankton in subtropical coastal waters showing lower thermal sensitivity than microzooplankton , 2018, Limnology and Oceanography.

[35]  A. Boetius,et al.  Microbial Communities in the East and West Fram Strait During Sea Ice Melting Season , 2018, Front. Mar. Sci..

[36]  P. Pearson,et al.  Temperature dependency of metabolic rates in the upper ocean: A positive feedback to global climate change? , 2018, Global and Planetary Change.

[37]  C. Hoppe,et al.  The Arctic picoeukaryote Micromonas pusilla benefits synergistically from warming and ocean acidification , 2018, Biogeosciences.

[38]  Wilken-Jon von Appen,et al.  Observations of a Submesoscale Cyclonic Filament in the Marginal Ice Zone , 2018, Geophysical Research Letters.

[39]  L. Oziel,et al.  Increased intrusion of warming Atlantic water leads to rapid expansion of temperate phytoplankton in the Arctic , 2018, Global change biology.

[40]  R. ffrench-Constant,et al.  Temperature‐driven selection on metabolic traits increases the strength of an algal–grazer interaction in naturally warmed streams , 2018, Global change biology.

[41]  E. Saiz,et al.  How much is enough for nutrients in microzooplankton dilution grazing experiments , 2018 .

[42]  Mridul K. Thomas,et al.  Individual-level trait diversity predicts phytoplankton community properties better than species richness or evenness , 2017, The ISME Journal.

[43]  A. Godhe,et al.  The role of intraspecific variation in the ecological and evolutionary success of diatoms in changing environments , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  P. Yager,et al.  Microbial Community Response to Terrestrially Derived Dissolved Organic Matter in the Coastal Arctic , 2017, Front. Microbiol..

[45]  S. Agustí,et al.  Thermal Thresholds of Phytoplankton Growth in Polar Waters and Their Consequences for a Warming Polar Ocean , 2017, Front. Mar. Sci..

[46]  M. Vernet,et al.  Models of Plankton Community Changes during a Warm Water Anomaly in Arctic Waters Show Altered Trophic Pathways with Minimal Changes in Carbon Export , 2017, Front. Mar. Sci..

[47]  Torsten Kanzow,et al.  Greater role for Atlantic inflows on sea-ice loss in the Eurasian Basin of the Arctic Ocean , 2017, Science.

[48]  A. Renner,et al.  The Atlantic Water boundary current north of Svalbard in late summer , 2017 .

[49]  Nico Boon,et al.  Measuring the biodiversity of microbial communities by flow cytometry , 2016 .

[50]  E. Buitenhuis,et al.  The Physiological Response of Picophytoplankton to Temperature and Its Model Representation , 2016, Front. Mar. Sci..

[51]  J. Guest,et al.  Design and Evaluation of Illumina MiSeq Compatible Primers for the 18S rRNA Gene for Improved Characterization of Mixed Microalgal Communities , 2016 .

[52]  Melanie Bergmann,et al.  Natural variability or anthropogenically-induced variation? Insights from 15 years of multidisciplinary observations at the arctic marine LTER site HAUSGARTEN , 2016 .

[53]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[54]  E. Nöthig,et al.  Biogeography and Photosynthetic Biomass of Arctic Marine Pico-Eukaroytes during Summer of the Record Sea Ice Minimum 2012 , 2016, PloS one.

[55]  Francisco M. Cornejo-Castillo,et al.  Global diversity and biogeography of deep-sea pelagic prokaryotes , 2015, The ISME Journal.

[56]  Bingzhang Chen Assessing the accuracy of the “two‐point” dilution technique , 2015 .

[57]  M. Cadotte,et al.  Predicting communities from functional traits. , 2015, Trends in ecology & evolution.

[58]  J. Berge,et al.  In the dark: A review of ecosystem processes during the Arctic polar night , 2015 .

[59]  E. Delong,et al.  Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre , 2015, Front. Microbiol..

[60]  P. Filzmoser,et al.  Bayesian-multiplicative treatment of count zeros in compositional data sets , 2015 .

[61]  E. Marañón Cell size as a key determinant of phytoplankton metabolism and community structure. , 2015, Annual review of marine science.

[62]  Astrid Bracher,et al.  Summertime plankton ecology in Fram Strait—a compilation of long- and short-term observations , 2015 .

[63]  C. Duarte,et al.  Experimental Assessment of Temperature Thresholds for Arctic Phytoplankton Communities , 2015, Estuaries and Coasts.

[64]  U. Riebesell,et al.  Between‐ and within‐population variations in thermal reaction norms of the coccolithophore Emiliania huxleyi , 2014 .

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

[66]  A. Engel,et al.  Regulation of bacterioplankton activity in Fram Strait (Arctic Ocean) during early summer: The role of organic matter supply and temperature , 2014 .

[67]  Elena Litchman,et al.  Marine Phytoplankton Temperature versus Growth Responses from Polar to Tropical Waters – Outcome of a Scientific Community-Wide Study , 2013, PloS one.

[68]  P. Eriksson,et al.  Recirculation in the Fram Strait and transports of water in and north of the Fram Strait derived from CTD data , 2013 .

[69]  Emilio Marañón,et al.  Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use. , 2013, Ecology letters.

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

[71]  Stéphane Audic,et al.  The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy , 2012, Nucleic Acids Res..

[72]  Elena Litchman,et al.  A Global Pattern of Thermal Adaptation in Marine Phytoplankton , 2012, Science.

[73]  Eberhard Fahrbach,et al.  Variability in Atlantic water temperature and transport at the entrance to the Arctic Ocean, 1997-2010 , 2012 .

[74]  Guy Woodward,et al.  Reconciling the temperature dependence of respiration across timescales and ecosystem types , 2012, Nature.

[75]  Hongbin Liu,et al.  Does warming enhance the effect of microzooplankton grazing on marine phytoplankton in the ocean? , 2012 .

[76]  C. M. Duarte,et al.  Temperature dependence of planktonic metabolism in the ocean , 2012 .

[77]  D. Vaulot,et al.  Composition of the summer photosynthetic pico and nanoplankton communities in the Beaufort Sea assessed by T-RFLP and sequences of the 18S rRNA gene from flow cytometry sorted samples , 2012, The ISME Journal.

[78]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[79]  Eduardo Costas,et al.  Warming will affect phytoplankton differently: evidence through a mechanistic approach , 2011, Proceedings of the Royal Society B: Biological Sciences.

[80]  H. Teeling,et al.  Complete genome sequence of Marinobacter adhaerens type strain (HP15), a diatom-interacting marine microorganism , 2010, Standards in genomic sciences.

[81]  A. Lopez-Urrutia,et al.  Increasing importance of small phytoplankton in a warmer ocean , 2010 .

[82]  M. Löder,et al.  Conserving original in situ diversity in microzooplankton grazing set-ups , 2010 .

[83]  Xiaodong Wang,et al.  Temperature effects on growth, colony development and carbon partitioning in three Phaeocystis species , 2010 .

[84]  R. Gerdes,et al.  Freshwater fluxes in the East Greenland Current: A decade of observations , 2009 .

[85]  E. Carmack,et al.  Smallest Algae Thrive As the Arctic Ocean Freshens , 2009, Science.

[86]  U. Sommer,et al.  Global warming benefits the small in aquatic ecosystems , 2009, Proceedings of the National Academy of Sciences.

[87]  A. Salamov,et al.  Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas , 2009, Science.

[88]  C. Pedrós-Alió,et al.  DISTRIBUTION, PHYLOGENY, AND GROWTH OF COLD‐ADAPTED PICOPRASINOPHYTES IN ARCTIC SEAS 1 , 2007 .

[89]  K. Hancke,et al.  Temperature effects on respiration and photosynthesis in three diatom-dominated benthic communities , 2004 .

[90]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[91]  D. Montagnes,et al.  Protists decrease in size linearly with temperature: ca. 2.5% °C−1 , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[92]  D. Kirchman The ecology of Cytophaga-Flavobacteria in aquatic environments. , 2002, FEMS microbiology ecology.

[93]  Peter J. Morin,et al.  Environmental warming alters food-web structure and ecosystem function , 1999, Nature.

[94]  P. Thompson,et al.  EFFECTS OF VARIATION IN TEMPERATURE. I. ON THE BIOCHEMICAL COMPOSITION OF EIGHT SPECIES OF MARINE PHYTOPLANKTON 1 , 1992 .

[95]  F. Millero,et al.  A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media , 1987 .

[96]  G. Kattner,et al.  Automatic method for the determination of ortho-phosphate and total dissolved phosphorus in the marine environment , 1987 .

[97]  C. Culberson,et al.  MEASUREMENT OF THE APPARENT DISSOCIATION CONSTANTS OF CARBONIC ACID IN SEAWATER AT ATMOSPHERIC PRESSURE1 , 1973 .

[98]  J. Strickland,et al.  The measurement of upwelling and subsequent biological process by means of the Technicon Autoanalyzer® and associated equipment , 1967 .