Control of phytoplankton-bacteria interactions by stoichiometric constraints

In aquatic ecosystems, phytoplanktonic organisms are the major primary producers and bacteria the major decomposers. The interactions between phytoplankton and bacteria may be dependent on nutrient resources. Anthropogenic inputs, by modifying nutrient status and stoichiometry of lakes, might induce changes in these interactions, and thus, could have many consequences on some ecological processes such as primary production or importance of microbial recycling activity. To test this hypothesis, we grew an axenic strain of a green alga, Scenedesmus obliquus, in a range of stoichiometric situations, in absence and in presence of a natural bacterial community. Here, we show that different phytoplankton limiting factors can generate between algae and bacteria either competition for nutrients in phosphorus-limited conditions, commensalism in nitrogen-limited conditions, or mutualism in eutrophic nutrient-unlimited conditions. Causes of these different interaction types are discussed, in particular the hypothesis that in very eutrophic systems with high primary production, mutualism between algae and bacteria could be due to CO2 supply by heterotrophic respiration to inorganic carbon limited algae. Some probable consequences for aquatic ecosystems functioning are proposed.

[1]  J. Mouget,et al.  Algal growth enhancement by bacteria: Is consumption of photosynthetic oxygen involved? , 1995 .

[2]  J. Cole.  Aquatic Microbiology for Ecosystem Scientists: New and Recycled Paradigms in Ecological Microbiology , 1999, Ecosystems.

[3]  S. Myklestad.  Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture , 1974 .

[4]  J. Elser,et al.  Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere , 2002 .

[5]  A. Kinzig,et al.  Mutualism and Competition between Plants and Decomposers: Implications for Nutrient Allocation in Ecosystems , 1993, The American Naturalist.

[6]  C. Duarte,et al.  Alkaline phosphatase activities in the central Atlantic Ocean indicate large areas with phosphorus deficiency , 2003 .

[7]  J. Elser,et al.  Element ratios and growth dynamics of bacteria in an oligotrophic Canadian shield lake , 1996 .

[8]  G. Bratbak,et al.  Phytoplankton-bacteria interactions: an apparant paradox? Analysis of a model system with both competition and commensalism , 1985 .

[9]  S. Carpenter,et al.  Influence of Food Web Structure on Carbon Exchange Between Lakes and the Atmosphere , 1997 .

[10]  Lennart Persson,et al.  Predator Regulation and Primary Production Along the Productivity Gradient of Temperate Lake Ecosystems , 1988 .

[11]  B. Biddanda,et al.  Small Players, Large Role: Microbial Influence on Biogeochemical Processes in Pelagic Aquatic Ecosystems , 2002, Ecosystems.

[12]  Robert W. Sterner,et al.  The Light: Nutrient Ratio in Lakes: The Balance of Energy and Materials Affects Ecosystem Structure and Process , 1997, The American Naturalist.

[13]  Michael L. Pace,et al.  The production of dissolved organic matter by phytoplankton and its importance to bacteria : patterns across marine and freshwater systems , 1991 .

[14]  Michel Loreau,et al.  Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  David J. Currie,et al.  A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus1 , 1984 .

[16]  M. Scheffer,et al.  Increase of atmospheric CO2 promotes phytoplankton productivity , 2004 .

[17]  J. Urabe,et al.  Regulation of the relationship between phytoplankton Scenedesmus acutus and heterotrophic bacteria by the balance of light and nutrients , 1999 .

[18]  I. Berman‐Frank,et al.  Balanced Growth in Aquatic Plants: Myth or Reality? , 1999 .

[19]  J. Fuhrman,et al.  Relationships between Biovolume and Biomass of Naturally Derived Marine Bacterioplankton. , 1987, Applied and environmental microbiology.

[20]  J. Elser,et al.  Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore , 2003 .

[21]  A. M. Johnston,et al.  Environmental regulation of CO2-concentrating mechanisms in microalgae , 1998 .

[22]  J. Noüe,et al.  Effect of acetate on growth and ammonium uptake in the microalga Scenedesmus obliquus , 1994 .

[23]  G. Kling,et al.  Carbon Dioxide Supersaturation in the Surface Waters of Lakes , 1994, Science.

[24]  J. Cotner,et al.  Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implications for growth- and resource-dependent variations , 2004 .

[25]  I. Obernosterer,et al.  Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N:P ratio , 1995 .

[26]  J. Huisman,et al.  Species Dynamics in Phytoplankton Blooms: Incomplete Mixing and Competition for Light , 1999, The American Naturalist.

[27]  D. Kreeger,et al.  COMBO: a defined freshwater culture medium for algae and zooplankton , 1998, Hydrobiologia.

[28]  M. Hein.  Inorganic carbon limitation of photosynthesis in lake phytoplankton , 1997 .

[29]  O. Vadstein,et al.  Can Phosphorus Limitation Inhibit Dissolved Organic Carbon Consumption in Aquatic Microbial Food Webs? A Study of Three Food Web Structures in Microcosms , 2002, Microbial Ecology.

[30]  J. Klug.  Bacterial response to dissolved organic matter affects resource availability for algae , 2005 .

[31]  M. Jansson.  Uptake, exchange and excretion of orthophosphate in phosphate‐starved Scenedesmus quadricauda and Pseudomonas K7 , 1993 .

[32]  G. Likens,et al.  Composition and Biomass of Phytoplankton , 2000 .

[33]  D. Kirchman,et al.  The uptake of inorganic nutrients by heterotrophic bacteria , 1994, Microbial Ecology.

[34]  Charles R. Goldman,et al.  Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America : a review and critique of experimental enrichments , 1990 .

[35]  E. Granéli,et al.  Molecular identification of bacteria associated with filaments of Nodularia spumigena and their effect on the cyanobacterial growth , 2003 .

[36]  I. Joint,et al.  Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms , 2002 .

[37]  Gérard Lacroix,et al.  Bacteria can control stoichiometry and nutrient limitation of phytoplankton , 2007 .

[38]  Jonathan J. Cole,et al.  INTERACTIONS BETWEEN BACTERIA AND ALGAE IN AQUATIC ECOSYSTEMS , 1982 .

[39]  R. Axler,et al.  Uses of alkaline phosphatase activity in evaluating phytoplankton community phosphorus deficiency , 1997, Hydrobiologia.

[40]  H. Knicker.  Stabilization of N-compounds in soil and organic-matter-rich sediments—what is the difference? , 2004 .

[41]  K. Porter,et al.  The use of DAPI for identifying and counting aquatic microflora1 , 1980 .

[42]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[43]  M. Loreau,et al.  ECOLOGICAL STOICHIOMETRY, PRIMARY PRODUCER-DECOMPOSER INTERACTIONS, AND ECOSYSTEM PERSISTENCE , 2001 .

[44]  G. Rhee,et al.  COMPETITION BETWEEN AN ALGA AND AN AQUATIC BACTERIUM FOR PHOSPHATE1 , 1972 .

[45]  Lydia Olander,et al.  Nitrogen and Nature , 2002, Ambio.

[46]  R. Pistocchi,et al.  Bacterial-algal interactions in polysaccharide production , 1998 .

[47]  O. Vadstein.  Heterotrophic, Planktonic Bacteria and Cycling of Phosphorus , 2000 .

[48]  J. Pernthaler,et al.  Effects of phosphorus loading on interactions of algae and bacteria: reinvestigation of the 'phytoplankton-bacteria paradox' in a continuous cultivation system , 2005 .