Acclimation to various temperature and pCO2 levels does not impact the competitive ability of two strains of Skeletonema marinoi in natural communities

Understanding the long-term response of key marine phytoplankton species to ongoing global changes is pivotal in determining how oceanic community composition will respond over the coming decades. To better understand the impact of ocean acidification and warming, we acclimated two strains of Skeletonema marinoi isolated from natural communities to three pCO2 (400 μatm, 600 μatm and 1000 μatm) for 8 months and five temperature conditions (7°C, 10°C, 13°C, 16°C and 19°C) for 11 months. These strains were then tested in natural microbial communities, exposed to three pCO2 treatments (400 μatm, 600 μatm and 1000 μatm). DNA metabarcoding of the 16S and 18S gene for prokaryotes and eukaryotes respectively was used to show differences in abundance and diversity between the three CO2 treatments. We found there were no significant differences in acclimated S. marinoi concentrations between the three pCO2 treatments, most likely due to the high variability these strains experience in their natural environment. There were significant compositional differences between the pCO2 treatments for prokaryotes suggesting that indirect changes to phytoplankton-bacteria interactions could be a possible driver of bacterial community composition. Yet, there were no differences for eukaryotic community composition, with all treatments dominated by diatoms (but not the acclimated S. marinoi) resulting in similar biodiversity. Furthermore, strain-specific differences in community composition suggests interactions between prokaryotic and eukaryotic taxa could play a role in determining future community composition.

[1]  Intergovernmental Panel on Climate Change (IPCC).  Climate Change 2022 – Impacts, Adaptation and Vulnerability , 2023 .

[2]  J. Hejzlar,et al.  Changes in nutrient concentration and water level affect the microbial loop: a 6-month mesocosm experiment , 2023, Aquatic Ecology.

[3]  C. Chiriac,et al.  The combined impact of low temperatures and shifting phosphorus availability on the competitive ability of cyanobacteria , 2022, Scientific Reports.

[4]  A. Godhe,et al.  Local adaptation through countergradient selection in northern populations of Skeletonema marinoi , 2022, Evolutionary applications.

[5]  L. Millet,et al.  Paleoreconstructions of ciliate communities reveal long-term ecological changes in temperate lakes , 2022, Scientific Reports.

[6]  S. Dupont,et al.  Upper environmental pCO2 drives sensitivity to ocean acidification in marine invertebrates , 2022, Nature Climate Change.

[7]  C. Chiriac,et al.  Long‐term acclimation might enhance the growth and competitive ability of Microcystis aeruginosa in warm environments , 2021, Freshwater Biology.

[8]  S. Dove,et al.  Tolerance to a highly variable environment does not infer resilience to future ocean warming and acidification in a branching coral , 2021, Limnology and Oceanography.

[9]  A. Allen,et al.  Microbial communities associated with sinking particles across an environmental gradient from coastal upwelling to the oligotrophic ocean , 2021, Deep Sea Research Part I: Oceanographic Research Papers.

[10]  Meng Chen,et al.  Nonribosomal peptide synthetases and nonribosomal cyanopeptides synthesis in Microcystis: A comparative genomics study , 2021 .

[11]  Tifeng Wang,et al.  Elevated pCO2 Impedes Succession of Phytoplankton Community From Diatoms to Dinoflagellates Along With Increased Abundance of Viruses and Bacteria , 2021, Frontiers in Marine Science.

[12]  N. Sato.  Are Cyanobacteria an Ancestor of Chloroplasts or Just One of the Gene Donors for Plants and Algae? , 2021, Genes.

[13]  Juntian Xu,et al.  Physiological responses of Skeletonema costatum to the interactions of seawater acidification and the combination of photoperiod and temperature , 2021 .

[14]  kwang-yul kim,et al.  Impact of climate change on the primary production and related biogeochemical cycles in the coastal and sea ice zone of the Southern Ocean. , 2021, The Science of the total environment.

[15]  Otto X. Cordero,et al.  Interactions between strains govern the eco-evolutionary dynamics of microbial communities , 2021, bioRxiv.

[16]  O. Ulloa,et al.  The Influence of pCO2-Driven Ocean Acidification on Open Ocean Bacterial Communities during A Short-Term Microcosm Experiment in the Eastern Tropical South Pacific (ETSP) off Northern Chile , 2020, Microorganisms.

[17]  Lisa T. Crummett,et al.  Acidification decreases microbial community diversity in the Salish Sea, a region with naturally high pCO2 , 2020, PloS one.

[18]  F. Figueroa,et al.  Short-term effects of increased CO2, nitrate and temperature on photosynthetic activity in Ulva rigida (Chlorophyta) estimated by different pulse amplitude modulated fluorometers and oxygen evolution. , 2020, Journal of experimental botany.

[19]  Atul K. Jain,et al.  Global Carbon Budget 2020 , 2020, Earth System Science Data.

[20]  J. Beardall,et al.  Combination of ocean acidification and warming enhances the competitive advantage of Skeletonema costatum over a green tide alga, Ulva linza. , 2019, Harmful algae.

[21]  A. Timmermann,et al.  Drivers of future seasonal cycle changes in oceanic pCO2 , 2018, Biogeosciences.

[22]  A. Godhe,et al.  A planktonic diatom displays genetic structure over small spatial scales , 2018, Environmental microbiology.

[23]  P. Tortell,et al.  Compensation of ocean acidification effects in Arctic phytoplankton assemblages , 2018, Nature Climate Change.

[24]  Otto X. Cordero,et al.  Strain-level diversity drives alternative community types in millimetre-scale granular biofilms , 2018, Nature Microbiology.

[25]  U. Riebesell,et al.  Simulated ocean acidification reveals winners and losers in coastal phytoplankton , 2017, PloS one.

[26]  J. Priscu,et al.  Early diverging lineages within Cryptomycota and Chytridiomycota dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys, Antarctica , 2017, Scientific Reports.

[27]  K. Gao,et al.  Effects of elevated CO2 on phytoplankton during a mesocosm experiment in the southern eutrophicated coastal water of China , 2017, Scientific Reports.

[28]  R. Stocker,et al.  Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships , 2017, Nature Microbiology.

[29]  U. Riebesell,et al.  Effects of ocean acidification on primary production in a coastal North Sea phytoplankton community , 2017, PloS one.

[30]  P. Thrall,et al.  Host species and environmental variation can influence rhizobial community composition , 2017 .

[31]  E. Achterberg,et al.  Ocean acidification impacts bacteria – phytoplankton coupling at low-nutrient conditions , 2017 .

[32]  R. Wanninkhof,et al.  Mapping of the air–sea CO2 flux in the Arctic Ocean and its adjacent seas: Basin-wide distribution and seasonal to interannual variability , 2016 .

[33]  C. Lovejoy,et al.  Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats , 2016, Scientific Reports.

[34]  J. McKinlay,et al.  Enhanced CO2 concentrations change the structure of Antarctic marine microbial communities , 2016 .

[35]  E. Calvo,et al.  Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2 , 2016 .

[36]  Kwang Young Kim,et al.  Effects of future climate conditions on photosynthesis and biochemical component of Ulva pertusa (Chlorophyta) , 2016 .

[37]  David A. Siegel,et al.  Revaluating ocean warming impacts on global phytoplankton , 2016 .

[38]  J. Jeffrey Morris,et al.  Impact of ocean acidification on the structure of future phytoplankton communities , 2015 .

[39]  J. Gattuso,et al.  Effect of ocean warming and acidification on a plankton community in the NW Mediterranean Sea , 2015 .

[40]  S. Dupont,et al.  Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod , 2015, Global change biology.

[41]  Ulrich Sommer,et al.  Warming and Ocean Acidification Effects on Phytoplankton—From Species Shifts to Size Shifts within Species in a Mesocosm Experiment , 2015, PloS one.

[42]  K. Gao,et al.  Photochemical responses of the diatom Skeletonema costatum grown under elevated CO2 concentrations to short-term changes in pH , 2015 .

[43]  P. Gouze,et al.  Diversity and geochemical structuring of bacterial communities along a salinity gradient in a carbonate aquifer subject to seawater intrusion. , 2014, FEMS microbiology ecology.

[44]  B. Worm,et al.  Effects of sea surface warming on marine plankton. , 2014, Ecology letters.

[45]  K. Gao,et al.  Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. , 2014, Functional plant biology : FPB.

[46]  I. Jonassen,et al.  Characterization of the 18S rRNA Gene for Designing Universal Eukaryote Specific Primers , 2014, PloS one.

[47]  Sinéad Collins,et al.  Evolutionary potential of marine phytoplankton under ocean acidification , 2013, Evolutionary applications.

[48]  E. W. Maas,et al.  Effect of ocean acidification on bacterial abundance, activity and diversity in the Ross Sea, Antarctica , 2013 .

[49]  Alexey A. Gurevich,et al.  QUAST: quality assessment tool for genome assemblies , 2013, Bioinform..

[50]  G. Bell,et al.  Long-term culture at elevated atmospheric CO2 fails to evoke specific adaptation in seven freshwater phytoplankton species , 2013, Proceedings of the Royal Society B: Biological Sciences.

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

[52]  U. Riebesell,et al.  Diurnal changes in seawater carbonate chemistry speciation at increasing atmospheric carbon dioxide , 2012, Marine biology.

[53]  U. Sommer,et al.  Phytoplankton response to a changing climate , 2012, Hydrobiologia.

[54]  Anders F. Andersson,et al.  Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea , 2011, The ISME Journal.

[55]  A. Körtzinger,et al.  Calcifying invertebrates succeed in a naturally CO 2 -rich coastal habitat but are threatened by high levels of future acidification , 2010 .

[56]  J. Middelburg,et al.  Phytoplankton-bacteria coupling under elevated CO 2 levels: a stable isotope labelling study , 2010 .

[57]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[58]  G. Nehrke,et al.  Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry , 2009 .

[59]  Jean-Pierre Gattuso,et al.  Technical Note: Approaches and software tools to investigate the impact of ocean acidification , 2009 .

[60]  L. Falcón,et al.  Dating the cyanobacterial ancestor of the chloroplast , 2009, The ISME Journal.

[61]  D. Hutchins,et al.  Effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response , 2009 .

[62]  D. Wolf-Gladrow,et al.  Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions , 2008 .

[63]  H. Paerl,et al.  Blooms Like It Hot , 2008, Science.

[64]  Kitack Lee,et al.  The effect of seawater CO 2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment , 1990 .

[65]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[66]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[67]  Jan Graffelman,et al.  Calibration of Multivariate Scatter plots for Exploratory Analysis of Relations Within and Between Sets of Variables in Genomic Research , 2005, Biometrical journal. Biometrische Zeitschrift.

[68]  C. Heip,et al.  Carbon‐nitrogen coupling and algal‐bacterial interactions during an experimental bloom: Modeling a 13C tracer experiment , 2004 .

[69]  K. Caldeira,et al.  Oceanography: Anthropogenic carbon and ocean pH , 2003, Nature.

[70]  D. Montagnes,et al.  Description of a New Marine Species of Askenasia Blochmann, 1895 (Ciliophora, Haptoria), With Notes on its Ecology , 2002, The Journal of eukaryotic microbiology.

[71]  Kenneth R. Hinga,et al.  Effects of pH on coastal marine phytoplankton , 2002 .

[72]  Frank J. Millero,et al.  Distribution of alkalinity in the surface waters of the major oceans , 1998 .

[73]  R. Warwick,et al.  Similarity-based testing for community pattern: the two-way layout with no replication , 1994 .

[74]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[75]  Iver W. Duedall,et al.  PREPARATION OF ARTIFICIAL SEAWATER1 , 1967 .

[76]  R. Guillard,et al.  Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. , 1962, Canadian journal of microbiology.

[77]  A. Kudryavtsev,et al.  A checklist of Amoebozoa species from marine and brackish-water biotopes with notes on taxonomy, species concept and distribution patterns , 2021, Protistology.

[78]  A. Waśkiewicz,et al.  Flavobacterium spp. – Characteristics, Occurrence, and Toxicity , 2014 .

[79]  B. Karlson,et al.  OVERVIEW OF COASTAL PHYTOPLANKTON INDICATORS AND THEIR POTENTIAL USE IN SWEDISH WATERS , 2013 .

[80]  B. Delille,et al.  Influence of giant kelp beds (Macrocystis pyrifera) on diel cycles of pCO2 and DIC in the Sub-Antarctic coastal area , 2009 .

[81]  R. Guillard,et al.  Culture of Phytoplankton for Feeding Marine Invertebrates , 1975 .