Impact of ocean phytoplankton diversity on phosphate uptake

Significance Nutrient uptake is a central property of ocean biogeochemistry, but our understanding of this process is based on laboratory cultures or bulk environmental studies. Thus, mathematical descriptions of nutrient uptake, at the heart of most biogeochemical models, must rely on this limited information. Hence, we have little knowledge of how natural phytoplankton populations vary in their abilities to take up key nutrients. Using advanced analytical techniques, this study provides the first comprehensive in situ quantification of nutrient uptake capabilities among dominant phytoplankton groups. Supported by a model that considers plastic ecological responses in an evolutionary context, this work further provides a fundamentally new framework for the integration of microbial diversity to describe and understand the controls of ocean nutrient assimilation. We have a limited understanding of the consequences of variations in microbial biodiversity on ocean ecosystem functioning and global biogeochemical cycles. A core process is macronutrient uptake by microorganisms, as the uptake of nutrients controls ocean CO2 fixation rates in many regions. Here, we ask whether variations in ocean phytoplankton biodiversity lead to novel functional relationships between environmental variability and phosphate (Pi) uptake. We analyzed Pi uptake capabilities and cellular allocations among phytoplankton groups and the whole community throughout the extremely Pi-depleted western North Atlantic Ocean. Pi uptake capabilities of individual populations were well described by a classic uptake function but displayed adaptive differences in uptake capabilities that depend on cell size and nutrient availability. Using an eco-evolutionary model as well as observations of in situ uptake across the region, we confirmed that differences among populations lead to previously uncharacterized relationships between ambient Pi concentrations and uptake. Supported by novel theory, this work provides a robust empirical basis for describing and understanding assimilation of limiting nutrients in the oceans. Thus, it demonstrates that microbial biodiversity, beyond cell size, is important for understanding the global cycling of nutrients.

[1]  S. Levin,et al.  Dynamic model of flexible phytoplankton nutrient uptake , 2011, Proceedings of the National Academy of Sciences.

[2]  Richard J. Geider,et al.  A dynamic regulatory model of phytoplanktonic acclimation to light, nutrients, and temperature , 1998 .

[3]  Maureen L. Coleman,et al.  Phosphate acquisition genes in Prochlorococcus ecotypes: Evidence for genome-wide adaptation , 2006, Proceedings of the National Academy of Sciences.

[4]  M. Lomas,et al.  Phytoplankton taxon-specific orthophosphate (Pi) and ATP utilization in the western subtropical North Atlantic , 2009 .

[5]  Susan M. Huse,et al.  Global Patterns of Bacterial Beta-Diversity in Seafloor and Seawater Ecosystems , 2011, PloS one.

[6]  J. Sharp,et al.  Determination of total dissolved phosphorus and particulate phosphorus in natural waters1 , 1980 .

[7]  K. Flynn Use, abuse, misconceptions and insights from quota models — the Droop cell quota model 40 years on , 2008 .

[8]  D. Karl,et al.  Microbial Group Specific Uptake Kinetics of Inorganic Phosphate and Adenosine-5′-Triphosphate (ATP) in the North Pacific Subtropical Gyre , 2012, Front. Microbio..

[9]  Jacques Monod,et al.  LA TECHNIQUE DE CULTURE CONTINUE THÉORIE ET APPLICATIONS , 1978 .

[10]  F. Morel,et al.  KINETICS OF NUTRIENT UPTAKE AND GROWTH IN PHYTOPLANKTON 1 , 1987 .

[11]  J. Grover INFLUENCE OF CELL SHAPE AND SIZE ON ALGAL COMPETITIVE ABILITY 1 , 1989 .

[12]  D. Capone,et al.  Phosphorus dynamics of the tropical and subtropical north Atlantic : Trichodesmium spp. versus bulk plankton , 2006 .

[13]  DAVID TITMAN,et al.  Ecological Competition Between Algae: Experimental Confirmation of Resource-Based Competition Theory , 1976, Science.

[14]  D. Canfield,et al.  Nitrogen in the Marine Environment , 2006 .

[15]  G. Rhee A CONTINUOUS CULTURE STUDY OF PHOSPHATE UPTAKE, GROWTH RATE AND POLYPHOSPHATE IN SCENEDESMUS SP. 1 , 1973 .

[16]  Adam C. Martiny,et al.  Widespread metabolic potential for nitrite and nitrate assimilation among Prochlorococcus ecotypes , 2009, Proceedings of the National Academy of Sciences.

[17]  Jasper A. Vrugt,et al.  Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter , 2013 .

[18]  Edward A. Boyle,et al.  Decoupling of iron and phosphate in the global ocean , 2005 .

[19]  Timothy R. Parsons,et al.  A manual of chemical and biological methods for seawater analysis , 1984 .

[20]  M. Zubkov,et al.  P‐affinity measurements of specific osmotroph populations using cell‐sorting flow cytometry , 2008 .

[21]  Melanie Abecassis,et al.  Ocean's least productive waters are expanding , 2008 .

[22]  J. C. Goldman,et al.  Chapter 7 – KINETICS OF INORGANIC NITROGEN UPTAKE BY PHYTOPLANKTON , 1983 .

[23]  M. R. Droop,et al.  Vitamin B12 and Marine Ecology. IV. The Kinetics of Uptake, Growth and Inhibition in Monochrysis Lutheri , 1968, Journal of the Marine Biological Association of the United Kingdom.

[24]  S. Doney,et al.  An intermediate complexity marine ecosystem model for the global domain , 2001 .

[25]  Richard C. Dugdale,et al.  NUTRIENT LIMITATION IN THE SEA: DYNAMICS, IDENTIFICATION, AND SIGNIFICANCE1 , 1967 .

[26]  Michael W. Lomas,et al.  Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP) , 2009 .

[27]  M. Follows,et al.  Optimal phytoplankton cell size in an allometric model , 2009 .

[28]  Mridul K. Thomas,et al.  Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton , 2012 .

[29]  A. Halpern,et al.  The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific , 2007, PLoS biology.

[30]  M. Lomas,et al.  Changes in partitioning of carbon amongst photosynthetic pico- and nano-plankton groups in the Sargasso Sea in response to changes in the North Atlantic Oscillation , 2013 .

[31]  I. Paulsen,et al.  Ecological Genomics of Marine Picocyanobacteria , 2009, Microbiology and Molecular Biology Reviews.

[32]  Sallie W. Chisholm,et al.  Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties , 1995 .

[33]  Jasper A. Vrugt,et al.  Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus , 2013, Proceedings of the National Academy of Sciences.

[34]  Richard Sanders,et al.  Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres , 2008 .

[35]  Peter Franks,et al.  Planktonic ecosystem models: perplexing parameterizations and a failure to fail , 2009 .

[36]  Paul G. Falkowski,et al.  Primary Productivity and Biogeochemical Cycles in the Sea , 1992 .

[37]  Fouad Badran,et al.  Improving the parameters of a global ocean biogeochemical model via variational assimilation of in situ data at five time series stations , 2011 .

[38]  Weizhong Li,et al.  Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. , 2009, Environmental microbiology.

[39]  M. Lomas,et al.  Dissolved inorganic and organic phosphorus uptake in Trichodesmium and the microbial community: The importance of phosphorus ester in the Sargasso Sea , 2010 .

[40]  S. Levin,et al.  A model for variable phytoplankton stoichiometry based on cell protein regulation , 2013 .

[41]  A. Devol,et al.  Nitrogen in the Marine Environment , 1985 .

[42]  G. Brasseur,et al.  Phosphorus Deficiency in the Atlantic:An Emerging Paradigm in Oceanography , 2003 .

[43]  D. Hutchins,et al.  A trace metal clean reagent to remove surface-bound iron from marine phytoplankton , 2003 .

[44]  R. Olson,et al.  Ultradian Growth in Prochlorococcus spp. , 1998, Applied and environmental microbiology.

[45]  S. Levin,et al.  Evolutionary comparison between viral lysis rate and latent period. , 2013, Journal of theoretical biology.