Emiliania huxleyi—Bacteria Interactions under Increasing CO2 Concentrations

Barcelos e Ramos, Joana; Ribeiro, Susana Chaves; Schulz, Kai George; Coelho, Francisco Jose Roso Da Costa; Oliveira, Vanessa; Cunha, Angela; Gomes, Newton Carlos Marcial; Brownlee, Colin; Passow, Uta; de Azevedo, Eduardo Brito

doi:10.3390/microorganisms10122461

Emiliania huxleyi—Bacteria Interactions under Increasing CO₂ Concentrations

Journal Article · Tue Dec 13 00:00:00 EST 2022 · Microorganisms

DOI:https://doi.org/10.3390/microorganisms10122461· OSTI ID:1908153

^[1]; ^[1]; Schulz, Kai George ^[2]; ^[3]; ^[3]; ^[3]; ^[3]; Brownlee, Colin ^[4]; Passow, Uta ^[5]; de Azevedo, Eduardo Brito ^[1]

University of the Azores, Angra do Heroísmo (Portugal)
Southern Cross University, Lismore, NSW (Australia)
University of Aveiro (Portugal)
Marine Biological Association of the United Kingdom, Plymouth (United Kingdom)
Memorial University of Newfoundland, St. John's, NL (Canada)

The interactions established between marine microbes, namely phytoplankton–bacteria, are key to the balance of organic matter export to depth and recycling in the surface ocean. Still, their role in the response of phytoplankton to rising CO₂ concentrations is poorly understood. Here, we show that the response of the cosmopolitan Emiliania huxleyi (E. huxleyi) to increasing CO₂ is affected by the coexistence with bacteria. Specifically, decreased growth rate of E. huxleyi at enhanced CO₂ concentrations was amplified in the bloom phase (potentially also related to nutrient concentrations) and with the coexistence with Idiomarina abyssalis (I. abyssalis) and Brachybacterium sp. In addition, enhanced CO₂ concentrations also affected E. huxleyi’s cellular content estimates, increasing organic and decreasing inorganic carbon, in the presence of I. abyssalis, but not Brachybacterium sp. At the same time, the bacterial isolates only survived in coexistence with E. huxleyi, but exclusively I. abyssalis at present CO₂ concentrations. Bacterial species or group-specific responses to the projected CO₂ rise, together with the concomitant effect on E. huxleyi, might impact the balance between the microbial loop and the export of organic matter, with consequences for atmospheric carbon dioxide.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Atmospheric Radiation Measurement (ARM) Data Center

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Contributing Organization:: Argonne National Laboratory (ANL); Brookhaven National Laboratory (BNL); Oak Ridge National Lab. (ORNL); Pacific Northwest National Laboratory (PNNL)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1908153

Journal Information:: Microorganisms, Journal Name: Microorganisms Journal Issue: 12 Vol. 10; ISSN 2076-2607

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (70)

Using SPAdes De Novo Assembler Prjibelski, Andrey; Antipov, Dmitry; Meleshko, Dmitry Current Protocols in Bioinformatics, Vol. 70, Issue 1 https://doi.org/10.1002/cpbi.102	journal	June 2020
Interactive effects of global climate change and pollution on marine microbes: the way ahead Coelho, Francisco J. R. C.; Santos, Ana L.; Coimbra, Joana Ecology and Evolution, Vol. 3, Issue 6 https://doi.org/10.1002/ece3.565	journal	April 2013
Diversity and community composition of particle-associated and free-living bacteria in mesopelagic and bathypelagic Southern Ocean water masses: Evidence of dispersal limitation in the Bransfield Strait: Bacteria in the deep Southern Ocean Milici, Mathias; Vital, Marius; Tomasch, Jürgen Limnology and Oceanography, Vol. 62, Issue 3 https://doi.org/10.1002/lno.10487	journal	February 2017
Bacteria-mediated aggregation of the marine phytoplankton Thalassiosira weissflogii and Nannochloropsis oceanica Tran, Nhan-An T.; Tamburic, Bojan; Evenhuis, Christian R. Journal of Applied Phycology, Vol. 32, Issue 6 https://doi.org/10.1007/s10811-020-02252-8	journal	September 2020
Effects of seawater acidification on hydrolytic enzyme activities Yamada, Namiha; Suzumura, Masahiro Journal of Oceanography, Vol. 66, Issue 2 https://doi.org/10.1007/s10872-010-0021-0	journal	March 2010
The effects of elevated carbon dioxide levels on a Vibrio sp. isolated from the deep-sea Labare, Michael P.; Bays, J. Timothy; Butkus, Michael A. Environmental Science and Pollution Research, Vol. 17, Issue 4 https://doi.org/10.1007/s11356-010-0297-z	journal	February 2010
Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results Clayton, Tonya D.; Byrne, Robert H. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 40, Issue 10 https://doi.org/10.1016/0967-0637(93)90048-8	journal	October 1993
Bacterial mediation of carbon fluxes during a diatom bloom in a mesocosm Smith, David C.; Steward, Grieg F.; Long, Richard A. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 42, Issue 1 https://doi.org/10.1016/0967-0645(95)00005-B	journal	January 1995
Vive la différence: plant functional diversity matters to ecosystem processes Dı́az, Sandra; Cabido, Marcelo Trends in Ecology & Evolution, Vol. 16, Issue 11 https://doi.org/10.1016/S0169-5347(01)02283-2	journal	November 2001
The origin of transparent exopolymer particles (TEP) and their role in the sedimentation of particulate matter Passow, U.; Shipe, R. F.; Murray, A. Continental Shelf Research, Vol. 21, Issue 4 https://doi.org/10.1016/S0278-4343(00)00101-1	journal	March 2001
Reference materials for oceanic CO2 analysis: a method for the certification of total alkalinity Dickson, A. G.; Afghan, J. D.; Anderson, G. C. Marine Chemistry, Vol. 80, Issue 2-3 https://doi.org/10.1016/S0304-4203(02)00133-0	journal	January 2003
A unifying concept of coccolithophore sensitivity to changing carbonate chemistry embedded in an ecological framework Bach, Lennart Thomas; Riebesell, Ulf; Gutowska, Magdalena A. Progress in Oceanography, Vol. 135 https://doi.org/10.1016/j.pocean.2015.04.012	journal	June 2015
Transparent exopolymer particles: Effects on carbon cycling in the ocean Mari, Xavier; Passow, Uta; Migon, Christophe Progress in Oceanography, Vol. 151 https://doi.org/10.1016/j.pocean.2016.11.002	journal	February 2017
Microbial mechanisms coupling carbon and phosphorus cycles in phosphorus-limited northern Adriatic Sea Malfatti, F.; Turk, V.; Tinta, T. Science of The Total Environment, Vol. 470-471 https://doi.org/10.1016/j.scitotenv.2013.10.040	journal	February 2014
Global-scale processes with a nanoscale drive: the role of marine viruses Brussaard, Corina P. D.; Wilhelm, Steven W.; Thingstad, Frede The ISME Journal, Vol. 2, Issue 6 https://doi.org/10.1038/ismej.2008.31	journal	April 2008
Respiration in the open ocean del Giorgio, Paul A.; Duarte, Carlos M. Nature, Vol. 420, Issue 6914 https://doi.org/10.1038/nature01165	journal	November 2002
The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis Seyedsayamdost, Mohammad R.; Case, Rebecca J.; Kolter, Roberto Nature Chemistry, Vol. 3, Issue 4 https://doi.org/10.1038/nchem.1002	journal	February 2011
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07641-9	journal	November 2018
Genome sequence of the deep-sea -proteobacterium Idiomarina loihiensis reveals amino acid fermentation as a source of carbon and energy Hou, S.; Saw, J. H.; Lee, K. S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 52 https://doi.org/10.1073/pnas.0407638102	journal	December 2004
Shifting the genomic gold standard for the prokaryotic species definition Richter, Michael; Rosselló-Móra, Ramon Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0906412106	journal	October 2009
Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea McCarren, J.; Becker, J. W.; Repeta, D. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 38 https://doi.org/10.1073/pnas.1010732107	journal	August 2010
Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics Bergauer, Kristin; Fernandez-Guerra, Antonio; Garcia, Juan A. L. Proceedings of the National Academy of Sciences, Vol. 115, Issue 3 https://doi.org/10.1073/pnas.1708779115	journal	December 2017
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison Richter, Michael; Rosselló-Móra, Ramon; Oliver Glöckner, Frank Bioinformatics, Vol. 32, Issue 6 https://doi.org/10.1093/bioinformatics/btv681	journal	November 2015
Versatile genome assembly evaluation with QUAST-LG Mikheenko, Alla; Prjibelski, Andrey; Saveliev, Vladislav Bioinformatics, Vol. 34, Issue 13 https://doi.org/10.1093/bioinformatics/bty266	journal	June 2018
Phylogeny.fr: robust phylogenetic analysis for the non-specialist Dereeper, A.; Guignon, V.; Blanc, G. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn180	journal	May 2008
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
dbCAN2: a meta server for automated carbohydrate-active enzyme annotation Zhang, Han; Yohe, Tanner; Huang, Le Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky418	journal	May 2018
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
OCEANOGRAPHY: Microbial Control of Oceanic Carbon Flux: The Plot Thickens Azam, F. Science, Vol. 280, Issue 5364 https://doi.org/10.1126/science.280.5364.694	journal	May 1998
Metagenome Survey of a Multispecies and Alga-Associated Biofilm Revealed Key Elements of Bacterial-Algal Interactions in Photobioreactors Krohn-Molt, Ines; Wemheuer, Bernd; Alawi, Malik Applied and Environmental Microbiology, Vol. 79, Issue 20 https://doi.org/10.1128/AEM.01641-13	journal	August 2013
Differing Growth Responses of Major Phylogenetic Groups of Marine Bacteria to Natural Phytoplankton Blooms in the Western North Pacific Ocean Tada, Yuya; Taniguchi, Akito; Nagao, Ippei Applied and Environmental Microbiology, Vol. 77, Issue 12 https://doi.org/10.1128/AEM.02952-10	journal	April 2011
Bacterial Secretion Systems: An Overview Green, Erin R.; Mecsas, Joan Microbiology Spectrum, Vol. 4, Issue 1 https://doi.org/10.1128/microbiolspec.VMBF-0012-2015	journal	February 2016
WebMGA: a customizable web server for fast metagenomic sequence analysis Wu, Sitao; Zhu, Zhengwei; Fu, Liming BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-444	journal	September 2011
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Stimulated Bacterial Growth under Elevated pCO2: Results from an Off-Shore Mesocosm Study Endres, Sonja; Galgani, Luisa; Riebesell, Ulf PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0099228	journal	June 2014
Elevated pCO2 enhances bacterioplankton removal of organic carbon James, Anna K.; Passow, Uta; Brzezinski, Mark A. PLOS ONE, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pone.0173145	journal	March 2017
Algae as an important environment for bacteria – phylogenetic relationships among new bacterial species isolated from algae Goecke, Franz; Thiel, Vera; Wiese, Jutta Phycologia, Vol. 52, Issue 1 https://doi.org/10.2216/12-24.1	journal	January 2013
The potential effects of global climate change on microalgal photosynthesis, growth and ecology Beardall, John; Raven, John A. Phycologia, Vol. 43, Issue 1 https://doi.org/10.2216/i0031-8884-43-1-26.1	journal	January 2004
Microbial dynamics in autotrophic and heterotrophic seawater mesocosms. III. Organic matter fluxes Grossart, H.; Engel, A.; Arnosti, C. Aquatic Microbial Ecology, Vol. 49 https://doi.org/10.3354/ame01140	journal	November 2007
Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning Liu, J.; Weinbauer, Mg; Maier, C. Aquatic Microbial Ecology, Vol. 61, Issue 3 https://doi.org/10.3354/ame01446	journal	December 2010
Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis, and Thalassiosira weissflogii) incubated under various conditions in the lab Grossart, Hp Aquatic Microbial Ecology, Vol. 19 https://doi.org/10.3354/ame019001	journal	January 1999
Microbial ecology of organic aggregates in aquatic ecosystems Simon, M.; Grossart, Hp; Schweitzer, B. Aquatic Microbial Ecology, Vol. 28 https://doi.org/10.3354/ame028175	journal	January 2002
The Ecological Role of Water-Column Microbes in the Sea Azam, F.; Fenchel, T.; Field, Jg Marine Ecology Progress Series, Vol. 10 https://doi.org/10.3354/meps010257	journal	January 1983
Effects of increased pCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response Feng, Y.; Hare, Ce; Leblanc, K. Marine Ecology Progress Series, Vol. 388 https://doi.org/10.3354/meps08133	journal	August 2009
Response of two marine bacterial isolates to high CO_{2 concentration} Teira, E.; Fernández, A.; Álvarez-Salgado, Xa Marine Ecology Progress Series, Vol. 453 https://doi.org/10.3354/meps09644	journal	May 2012
Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption Engel, A.; Passow, U. Marine Ecology Progress Series, Vol. 219 https://doi.org/10.3354/meps219001	journal	January 2001
Expanding the World of Marine Bacterial and Archaeal Clades Yilmaz, Pelin; Yarza, Pablo; Rapp, Josephine Z. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01524	journal	January 2016
Bacterial Succession on Sinking Particles in the Ocean's Interior Pelve, Erik A.; Fontanez, Kristina M.; DeLong, Edward F. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02269	journal	November 2017
Bacterial Communities of Diatoms Display Strong Conservation Across Strains and Time Behringer, Gregory; Ochsenkühn, Michael A.; Fei, Cong Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00659	journal	April 2018
Drivers of Regional Bacterial Community Structure and Diversity in the Northwest Atlantic Ocean Zorz, Jackie; Willis, Ciara; Comeau, André M. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00281	journal	February 2019
Measurement of the Apparent Dissociation Constants of Carbonic acid in Seawater at Atmospheric Pressure1 Mehrbach, C.; Culberson, C. H.; Hawley, J. E. Limnology and Oceanography, Vol. 18, Issue 6 https://doi.org/10.4319/lo.1973.18.6.0897	journal	November 1973
Improved analysis for “particulate” organic carbon and nitrogen from seawater1 Sharp, Jonathan H. Limnology and Oceanography, Vol. 19, Issue 6 https://doi.org/10.4319/lo.1974.19.6.0984	journal	November 1974
Microbial degradation of organic carbon and nitrogen on diatom aggregates Grossart, Hans-Peter; Ploug, Helle Limnology and Oceanography, Vol. 46, Issue 2 https://doi.org/10.4319/lo.2001.46.2.0267	journal	March 2001
Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton Grossart, Hans-Peter; Allgaier, Martin; Passow, Uta Limnology and Oceanography, Vol. 51, Issue 1 https://doi.org/10.4319/lo.2006.51.1.0001	journal	January 2006
Considerations for the measurement of spectrophotometric pH for ocean acidification and other studies DeGrandpre, Mike D.; Spaulding, Reggie S.; Newton, Jenny O. Limnology and Oceanography: Methods, Vol. 12, Issue 12 https://doi.org/10.4319/lom.2014.12.830	journal	December 2014
Response of bacterioplankton activity in an Arctic fjord system to elevated p CO 2 : results from a mesocosm perturbation study Piontek, J.; Borchard, C.; Sperling, M. Biogeosciences, Vol. 10, Issue 1 https://doi.org/10.5194/bg-10-297-2013	journal	January 2013
Ocean acidification shows negligible impacts on high-latitude bacterial community structure in coastal pelagic mesocosms Roy, A. -S.; Gibbons, S. M.; Schunck, H. Biogeosciences, Vol. 10, Issue 1 https://doi.org/10.5194/bg-10-555-2013	journal	January 2013
Arctic microbial community dynamics influenced by elevated CO 2 levels Brussaard, C. P. D.; Noordeloos, A. A. M.; Witte, H. Biogeosciences, Vol. 10, Issue 2 https://doi.org/10.5194/bg-10-719-2013	journal	January 2013
Reviews and Syntheses: Responses of coccolithophores to ocean acidification: a meta-analysis Meyer, J.; Riebesell, U. Biogeosciences, Vol. 12, Issue 6 https://doi.org/10.5194/bg-12-1671-2015	journal	January 2015
Coupling of heterotrophic bacteria to phytoplankton bloom development at different p CO 2 levels: a mesocosm study Allgaier, M.; Riebesell, U.; Vogt, M. Biogeosciences, Vol. 5, Issue 4 https://doi.org/10.5194/bg-5-1007-2008	journal	January 2008
Availability of phosphate for phytoplankton and bacteria and of glucose for bacteria at different p CO 2 levels in a mesocosm study Tanaka, T.; Thingstad, T. F.; Løvdal, T. Biogeosciences, Vol. 5, Issue 3 https://doi.org/10.5194/bg-5-669-2008	journal	January 2008
Build-up and decline of organic matter during PeECE III Schulz, K. G.; Riebesell, U.; Bellerby, R. G. J. Biogeosciences, Vol. 5, Issue 3 https://doi.org/10.5194/bg-5-707-2008	journal	May 2008
CO₂ perturbation experiments: similarities and differences between dissolved inorganic carbon and total alkalinity manipulations Schulz, K. G.; Barcelos e. Ramos, J.; Zeebe, R. E. Biogeosciences, Vol. 6, Issue 10 https://doi.org/10.5194/bg-6-2145-2009	journal	October 2009
Acidification increases microbial polysaccharide degradation in the ocean Piontek, J.; Lunau, M.; Händel, N. Biogeosciences, Vol. 7, Issue 5 https://doi.org/10.5194/bg-7-1615-2010	journal	January 2010
Short-term response of the coccolithophore Emiliania huxleyi to an abrupt change in seawater carbon dioxide concentrations Barcelos e. Ramos, J.; Müller, M. N.; Riebesell, U. Biogeosciences, Vol. 7, Issue 1 https://doi.org/10.5194/bg-7-177-2010	journal	January 2010
Organic matter exudation by Emiliania huxleyi under simulated future ocean conditions Borchard, C.; Engel, A. Biogeosciences, Vol. 9, Issue 8 https://doi.org/10.5194/bg-9-3405-2012	journal	January 2012
Influence of changing carbonate chemistry on morphology and weight of coccoliths formed by Emiliania huxleyi Bach, L. T.; Bauke, C.; Meier, K. J. S. Biogeosciences, Vol. 9, Issue 8 https://doi.org/10.5194/bg-9-3449-2012	journal	August 2012

Similar Records

Change in Emiliania huxleyi Virus Assemblage Diversity but Not in Host Genetic Composition during an Ocean Acidification Mesocosm Experiment

Journal Article · Tue Feb 28 19:00:00 EST 2017 · Viruses · OSTI ID:1628596

A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic

Journal Article · Tue Nov 30 23:00:00 EST 1993 · Global Biogeochemical Cycles; (United States) · OSTI ID:7010104

The Bacterial Symbiont Phaeobacter inhibens Shapes the Life History of Its Algal Host Emiliania huxleyi

Journal Article · Mon May 28 20:00:00 EDT 2018 · Frontiers in Marine Science · OSTI ID:1477299

Related Subjects

54 ENVIRONMENTAL SCIENCES
Brachybacterium sp.
CO2
Emiliania huxleyi
Idiomarina abyssalis
changing ocean
coccolithophores
functional profiling of marine bacteria
phytoplankton–bacteria interactions

Emiliania huxleyi—Bacteria Interactions under Increasing CO2 Concentrations

Citation Formats

References (70)

Similar Records

Related Subjects

Emiliania huxleyi—Bacteria Interactions under Increasing CO₂ Concentrations