Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Arandia-Gorostidi, Nestor; Weber, Peter K.; Alonso-Sáez, Laura; Morán, Xosé Anxelu G.; Mayali, Xavier

doi:10.1038/ismej.2016.156

Title: Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Journal Article · Mon Dec 05 23:00:00 EST 2016 · The ISME Journal

DOI: https://doi.org/10.1038/ismej.2016.156 · OSTI ID:1351131

Arandia-Gorostidi, Nestor ^[1]; Weber, Peter K. ^[2]; Alonso-Sáez, Laura ^[3]; Morán, Xosé Anxelu G. ^[4]; Mayali, Xavier ^[5]

Centro Oceanografico de Gijon/Xixon, Asturias (Spain)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Centro Oceanografico de Gijon/Xixon, Asturias (Spain); AZTI, Bizkaia (Spain)
Centro Oceanografico de Gijon/Xixon, Asturias (Spain); King Abdullah Univ. of Science and Technology, Thuwal (Saudi Arabia)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Oregon State Univ., Corvallis, OR (United States)

Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4 °C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Lastly, our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1351131

Report Number(s):: LLNL-JRNL--677811

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 3 Vol. 11; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Links between Phytoplankton and Bacterial Community Dynamics in a Coastal Marine Environment Rooney-Varga, J. N.; Giewat, M. W.; Savin, M. C. Microbial Ecology, Vol. 49, Issue 1 https://doi.org/10.1007/s00248-003-1057-0	journal	January 2005
Turbulence and the diffusive layers around small organisms Lazier, J. R. N.; Mann, K. H. Deep Sea Research Part A. Oceanographic Research Papers, Vol. 36, Issue 11 https://doi.org/10.1016/0198-0149(89)90068-X	journal	November 1989
Molecular identification of bacteria associated with filaments of Nodularia spumigena and their effect on the cyanobacterial growth Salomon, Paulo S.; Janson, Sven; Granéli, Edna Harmful Algae, Vol. 2, Issue 4 https://doi.org/10.1016/S1568-9883(03)00045-3	journal	October 2003
Photosynthetic parameters and primary production, with focus on large phytoplankton, in a temperate mid-shelf ecosystem Morán, Xosé Anxelu G.; Scharek, Renate Estuarine, Coastal and Shelf Science, Vol. 154 https://doi.org/10.1016/j.ecss.2014.12.047	journal	March 2015
Utilisation of leucine by several phytoplankton species Kamjunke, Norbert; Tittel, Jörg Limnologica, Vol. 38, Issue 3-4 https://doi.org/10.1016/j.limno.2008.05.002	journal	October 2008
Heterotrophic and mixotrophic growth of Micractinium pusillum Fresenius in the presence of acetate and glucose:effect of light and acetate gradient concentration Bouarab, L.; Dauta, A.; Loudiki, M. Water Research, Vol. 38, Issue 11 https://doi.org/10.1016/j.watres.2004.03.021	journal	June 2004
Response of ocean ecosystems to climate warming Sarmiento, J. L.; Slater, R.; Barber, R. Global Biogeochemical Cycles, Vol. 18, Issue 3 https://doi.org/10.1029/2003GB002134	journal	July 2004
Sea snow microcosms Azam, Farooq; Long, Richard A. Nature, Vol. 414, Issue 6863 https://doi.org/10.1038/35107174	journal	November 2001
Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides Popa, Radu; Weber, Peter K.; Pett-Ridge, Jennifer The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.44	journal	July 2007
Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii Gärdes, Astrid; Iversen, Morten H.; Grossart, Hans-Peter The ISME Journal, Vol. 5, Issue 3 https://doi.org/10.1038/ismej.2010.145	journal	September 2010
Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean Jardillier, Ludwig; Zubkov, Mikhail V.; Pearman, John The ISME Journal, Vol. 4, Issue 9 https://doi.org/10.1038/ismej.2010.36	journal	April 2010
N2-fixation, ammonium release and N-transfer to the microbial and classical food web within a plankton community Adam, Birgit; Klawonn, Isabell; Svedén, Jennie B. The ISME Journal, Vol. 10, Issue 2 https://doi.org/10.1038/ismej.2015.126	journal	August 2015
Global distribution and vertical patterns of a prymnesiophyte–cyanobacteria obligate symbiosis Cabello, Ana M.; Cornejo-Castillo, Francisco M.; Raho, Nicolas The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.147	journal	September 2015
Algae acquire vitamin B12 through a symbiotic relationship with bacteria Croft, Martin T.; Lawrence, Andrew D.; Raux-Deery, Evelyne Nature, Vol. 438, Issue 7064 https://doi.org/10.1038/nature04056	journal	November 2005
Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria Amin, S. A.; Hmelo, L. R.; van Tol, H. M. Nature, Vol. 522, Issue 7554 https://doi.org/10.1038/nature14488	journal	May 2015
Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton Cornejo-Castillo, Francisco M.; Cabello, Ana M.; Salazar, Guillem Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11071	journal	March 2016
Microbial structuring of marine ecosystems Azam, Farooq; Malfatti, Francesca Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1747	journal	October 2007
Master recyclers: features and functions of bacteria associated with phytoplankton blooms Buchan, Alison; LeCleir, Gary R.; Gulvik, Christopher A. Nature Reviews Microbiology, Vol. 12, Issue 10 https://doi.org/10.1038/nrmicro3326	journal	August 2014
Inhibition kinetics of nitrate uptake by ammonium in size-fractionated oceanic phytoplankton communities: implications for new production and f-ratio estimates L'Helguen, S.; Maguer, J. -F.; Caradec, J. Journal of Plankton Research, Vol. 30, Issue 10 https://doi.org/10.1093/plankt/fbn072	journal	July 2008
Importance of dissolved organic carbon for phytoplankton nutrition in a eutrophic reservoir Znachor, P.; Nedoma, J. Journal of Plankton Research, Vol. 32, Issue 3 https://doi.org/10.1093/plankt/fbp129	journal	December 2009
Effects of sea surface warming on the production and composition of dissolved organic matter during phytoplankton blooms: results from a mesocosm study Engel, A.; Handel, N.; Wohlers, J. Journal of Plankton Research, Vol. 33, Issue 3 https://doi.org/10.1093/plankt/fbq122	journal	September 2010
Annual cycles of bacterioplankton biomass and production suggest a general switch between temperature and resource control in temperate coastal ecosystems Calvo-Díaz, Alejandra; Franco-Vidal, Leticia; Morán, Xosé Anxelu G. Journal of Plankton Research, Vol. 36, Issue 3 https://doi.org/10.1093/plankt/fbu022	journal	March 2014
More, smaller bacteria in response to ocean's warming? Morán, Xosé Anxelu G.; Alonso-Sáez, Laura; Nogueira, Enrique Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1810 https://doi.org/10.1098/rspb.2015.0371	journal	July 2015
Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Sarmento, Hugo; Montoya, José M.; Vázquez-Domínguez, Evaristo Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1549 https://doi.org/10.1098/rstb.2010.0045	journal	July 2010
Impact of warming on phyto-bacterioplankton coupling and bacterial community composition in experimental mesocosms: Temperature impact on phyto-bacterioplankton coupling von Scheibner, Markus; Dörge, Petra; Biermann, Antje Environmental Microbiology, Vol. 16, Issue 3 https://doi.org/10.1111/1462-2920.12195	journal	July 2013
Diurnal variations in the auto- and heterotrophic activity of cyanobacterial phycospheres (Gloeotrichia echinulata) and the identity of attached bacteria Eiler, Alexander; Olsson, Jan A.; Bertilsson, Stefan Freshwater Biology, Vol. 51, Issue 2 https://doi.org/10.1111/j.1365-2427.2005.01493.x	journal	February 2006
Ocean warming enhances respiration and carbon demand of coastal microbial plankton VÁZquez-DomÍNguez, Evaristo; VaquÉ, Dolors; Gasol, Josep M. Global Change Biology, Vol. 13, Issue 7 https://doi.org/10.1111/j.1365-2486.2007.01377.x	journal	July 2007
Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages Grossart, Hans-Peter; Tang, Kam W.; KiÃ¸rboe, Thomas FEMS Microbiology Letters, Vol. 266, Issue 2 https://doi.org/10.1111/j.1574-6968.2006.00520.x	journal	January 2007
Unicellular Cyanobacterium Symbiotic with a Single-Celled Eukaryotic Alga Thompson, A. W.; Foster, R. A.; Krupke, A. Science, Vol. 337, Issue 6101 https://doi.org/10.1126/science.1222700	journal	September 2012
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
Light-Stimulated Bacterial Production and Amino Acid Assimilation by Cyanobacteria and Other Microbes in the North Atlantic Ocean Michelou, V. K.; Cottrell, M. T.; Kirchman, D. L. Applied and Environmental Microbiology, Vol. 73, Issue 17 https://doi.org/10.1128/AEM.00212-07	journal	July 2007
Bacterial dry matter content and biomass estimations. Bratbak, G.; Dundas, I. Applied and Environmental Microbiology, Vol. 48, Issue 4 https://doi.org/10.1128/AEM.48.4.755-757.1984	journal	January 1984
Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Kirchman, D.; K'nees, E.; Hodson, R. Applied and Environmental Microbiology, Vol. 49, Issue 3 https://doi.org/10.1128/AEM.49.3.599-607.1985	journal	January 1985
Dynamics of Bacterial Community Composition and Activity during a Mesocosm Diatom Bloom Riemann, L.; Steward, G. F.; Azam, F. Applied and Environmental Microbiology, Vol. 66, Issue 2 https://doi.org/10.1128/AEM.66.2.578-587.2000	journal	February 2000
High Rate of Uptake of Organic Nitrogen Compounds by Prochlorococcus Cyanobacteria as a Key to Their Dominance in Oligotrophic Oceanic Waters Zubkov, M. V.; Fuchs, B. M.; Tarran, G. A. Applied and Environmental Microbiology, Vol. 69, Issue 2 https://doi.org/10.1128/AEM.69.2.1299-1304.2003	journal	February 2003
Interactions between Diatoms and Bacteria Amin, S. A.; Parker, M. S.; Armbrust, E. V. Microbiology and Molecular Biology Reviews, Vol. 76, Issue 3 https://doi.org/10.1128/MMBR.00007-12	journal	August 2012
The Oligotrophic Ocean Is Heterotrophic Duarte, Carlos M.; Regaudie-de-Gioux, Aurore; Arrieta, Jesús M. Annual Review of Marine Science, Vol. 5, Issue 1 https://doi.org/10.1146/annurev-marine-121211-172337	journal	January 2013
Single-Cell Ecophysiology of Microbes as Revealed by Raman Microspectroscopy or Secondary Ion Mass Spectrometry Imaging Wagner, Michael Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073233	journal	October 2009
Sunlight Effects on the Osmotrophic Uptake of DMSP-Sulfur and Leucine by Polar Phytoplankton Ruiz-González, Clara; Galí, Martí; Sintes, Eva PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0045545	journal	September 2012
Resource Limitation of Bacterial Production Distorts the Temperature Dependence of Oceanic Carbon Cycling López-Urrutia, Ángel; Morán, Xosé Anxelu G. Ecology, Vol. 88, Issue 4 https://doi.org/10.1890/06-1641	journal	April 2007
Chemotactic and Growth Responses of Marine Bacteria to Algal Extracellular Products Bell, Wayne; Mitchell, Ralph The Biological Bulletin, Vol. 143, Issue 2 https://doi.org/10.2307/1540052	journal	October 1972
Primary production, biomass and abundance of phototrophic picoplankton in the Mediterranean Sea: a review Magazzù, G.; Decembrini, F. Aquatic Microbial Ecology, Vol. 9 https://doi.org/10.3354/ame009097	journal	January 1995
Major and comparable roles for free-living and attached bacteria in the degradation of Phaeocystis-derived organic matter in Belgian coastal waters of the North Sea Becquevort, S.; Rousseau, V.; Lancelot, C. Aquatic Microbial Ecology, Vol. 14 https://doi.org/10.3354/ame014039	journal	January 1998
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
Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay Calvo-Díaz, A.; Morán, Xag Aquatic Microbial Ecology, Vol. 42 https://doi.org/10.3354/ame042159	journal	January 2006
Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics Grossart, Hp; Simon, M. Aquatic Microbial Ecology, Vol. 47 https://doi.org/10.3354/ame047163	journal	May 2007
Environmental control of nitrate and ammonium uptake by phytoplankton in the Equatorial Atlantic Ocean Le Bouteiller, A. Marine Ecology Progress Series, Vol. 30 https://doi.org/10.3354/meps030167	journal	January 1986
Temperature effects on the growth rate of marine picoplankton Chen, B.; Liu, H.; Huang, B. Marine Ecology Progress Series, Vol. 505 https://doi.org/10.3354/meps10773	journal	May 2014
Measurement of nitrate and ammonium uptake at ambient concentrations in oligotrophic waters of the North-East Atlantic Ocean Rees, A.; Woodward, M.; Joint, I. Marine Ecology Progress Series, Vol. 187 https://doi.org/10.3354/meps187295	journal	January 1999
Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments Marañón, E.; Holligan, Pm; Barciela, R. Marine Ecology Progress Series, Vol. 216 https://doi.org/10.3354/meps216043	journal	January 2001
Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities [Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities] Gasol, Josep M.; Del Giorgio, Paul A. Scientia Marina, Vol. 64, Issue 2 https://doi.org/10.3989/scimar.2000.64n2197	journal	June 2000
Simulating chemosensory responses of marine microorganisms1: Bacterial chemokinesis Jackson, George A. Limnology and Oceanography, Vol. 32, Issue 6 https://doi.org/10.4319/lo.1987.32.6.1253	journal	November 1987
The kinetics of nitrogen utilization in the oceanic mixed layer: Nitrate and ammonium interactions at nanomolar concentrations Harrison, W. G.; Harris, L. R.; Irwin, B. D. Limnology and Oceanography, Vol. 41, Issue 1 https://doi.org/10.4319/lo.1996.41.1.0016	journal	January 1996
Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production Agawin, Nona S. R.; Duarte, Carlos M.; Agustí, Susana Limnology and Oceanography, Vol. 45, Issue 8 https://doi.org/10.4319/lo.2000.45.8.1891a	journal	December 2000
Response of Southern Ocean phytoplankton and bacterioplankton production to short-term experimental warming MorÁn, XosÉ Anxelu G.; SebastiÁn, Marta; Pedrís-Alií, Carlos Limnology and Oceanography, Vol. 51, Issue 4 https://doi.org/10.4319/lo.2006.51.4.1791	journal	July 2006
Large-scale variability in surface bacterial carbon demand and growth efficiency in the subtropical northeast Atlantic Ocean Alonso-Sáez, Laura; Gasol, Josep M.; Arístegui, Javier Limnology and Oceanography, Vol. 52, Issue 2 https://doi.org/10.4319/lo.2007.52.2.0533	journal	March 2007
Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a northeastern Pacific inshore-offshore transect del Giorgio, Paul A.; Condon, Robert; Bouvier, Thierry Limnology and Oceanography, Vol. 56, Issue 1 https://doi.org/10.4319/lo.2011.56.1.0001	journal	November 2010
Low microbial respiration of leucine at ambient oceanic concentration in the mixed layer of the central Atlantic Ocean Hill, Polly G.; Warwick, Phillip E.; Zubkov, Mikhail V. Limnology and Oceanography, Vol. 58, Issue 5 https://doi.org/10.4319/lo.2013.58.5.1597	journal	July 2013
Seasonal to hour variation scales in abundance and production of total and particle-attached bacteria in the open NW Mediterranean Sea (0–1000 m) Mével, G.; Vernet, M.; Goutx, M. Biogeosciences, Vol. 5, Issue 6 https://doi.org/10.5194/bg-5-1573-2008	journal	January 2008

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