Stoichiometric Constraints on Resource Use, Competitive Interactions, and Elemental Cycling in Microbial Decomposers

Heterotrophic microbial decomposers, such as bacteria and fungi, immobilize or mineralize inorganic elements, depending on their elemental composition and that of their organic resource. This fact has major implications for their interactions with other consumers of inorganic elements. We combine the stoichiometric and resource‐ratio approaches in a model describing the use by decomposers of an organic and an inorganic resource containing the same essential element, to study its consequences on decomposer interactions and their role in elemental cycling. Our model considers the elemental composition of organic matter and the principle of its homeostasis explicitly. New predictions emerge, in particular, (1) stoichiometric constraints generate a trade‐off between the R* values of decomposers for the two resources; (2) they create favorable conditions for the coexistence of decomposers limited by different resources and with different elemental demands; (3) however, combined with conditions on species‐specific equilibrium limitation, they draw decomposers toward colimitation by the organic and inorganic resources on an evolutionary time scale. Moreover, we derive the conditions under which decomposers switch from consumption to excretion of the inorganic resource. We expect our predictions to be useful in explaining the community structure of decomposers and their interactions with other consumers of inorganic resources, particularly primary producers.

[1]  J. Cole,et al.  BACTERIAL GROWTH EFFICIENCY IN NATURAL AQUATIC SYSTEMS , 1998 .

[2]  J. C. Goldman,et al.  Growth of marine bacteria in batch and continuous culture under carbon and nitrogen limitation , 2000 .

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

[4]  James P Grover,et al.  Stoichiometry, herbivory and competition for nutrients: simple models based on planktonic ecosystems. , 2002, Journal of theoretical biology.

[5]  J. Vallino,et al.  Modeling bacterial utilization of dissolved organic matter: Optimization replaces Monod growth kinetics , 1996 .

[6]  David Tilman,et al.  Resources: A Graphical-Mechanistic Approach to Competition and Predation , 1980, The American Naturalist.

[7]  Nicolas Mouquet,et al.  A Critical Review of Twenty Years’ Use of the Resource‐Ratio Theory , 2005, The American Naturalist.

[8]  V. Smith Applicability of resource-ratio theory to microbial ecology , 1993 .

[9]  M. Jansson,et al.  Bacterioplankton Growth and Nutrient Use Efficiencies Under Variable Organic Carbon and Inorganic Phosphorus Ratios , 2006, Microbial Ecology.

[10]  H. Parnas Model for decomposition of organic material by microorganisms , 1975 .

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

[12]  O. Vadstein Evaluation of competitive ability of two heterotrophic planktonic bacteria under phosphorus limitation , 1998 .

[13]  O. AndreÂna,et al.  Biodiversity and soil functioningÐfrom black box to can of worms ? , 1999 .

[14]  B. Dreyfus,et al.  Do concentrations of glucose and fungal inoculum influence the competitiveness of two early-stage ectomycorrhizal fungi in Afzelia africana seedlings? , 2004 .

[15]  L. Legendre,et al.  MODEL OF BACTERIAL GROWTH INFLUENCED BY SUBSTRATE C:N RATIO AND CONCENTRATION , 1999 .

[16]  Yang Kuang,et al.  Competition and stoichiometry: coexistence of two predators on one prey. , 2004, Theoretical population biology.

[17]  T. Thingstad,et al.  Fate and effect of allochthonous organic material in aquatic microbial ecosystems An analysis based on chemostat theory , 1985 .

[18]  A. C. R. Dean,et al.  Continuous culture 6. Applications and new fields. , 1976 .

[19]  T. Egli,et al.  Dual nutrient limited growth: models, experimental observations, and applications. , 2004, Journal of biotechnology.

[20]  Katarina Vrede,et al.  Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton , 2002, Applied and Environmental Microbiology.

[21]  F. T.,et al.  Phytoplankton-bacteria interactions : an apparent paradox ? Analysis of a model system with both competition and commensalism , 2006 .

[22]  N. Basson Competition for glucose between Candida albicans and oral bacteria grown in mixed culture in a chemostat. , 2000, Journal of medical microbiology.

[23]  E. Bååth,et al.  Influence of Initial C/N Ratio on Chemical and Microbial Composition during Long Term Composting of Straw , 2001, Microbial Ecology.

[24]  J. C. Goldman,et al.  Ammonium regeneration and carbon utilization by marine bacteria grown on mixed substrates , 1991 .

[25]  Allen G. Marr,et al.  THE MAINTENANCE REQUIREMENT OF ESCHERICHIA COLI , 1963 .

[26]  D. Tilman A Consumer-Resource Approach to Community Structure , 1986 .

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

[28]  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 .

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

[30]  J. Elser,et al.  FUNDAMENTAL CONNECTIONS AMONG ORGANISM C:N:P STOICHIOMETRY, MACROMOLECULAR COMPOSITION, AND GROWTH , 2004 .

[31]  Robert W. Sterner,et al.  Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C : N : P stoichiometry , 2003 .

[32]  G. Lamberti,et al.  Taxonomic and regional patterns in benthic macroinvertebrate elemental composition in streams , 2005 .

[33]  S. Hall Stoichiometrically Explicit Competition between Grazers: Species Replacement, Coexistence, and Priority Effects along Resource Supply Gradients , 2004, The American Naturalist.

[34]  David Tilman,et al.  Tests of Resource Competition Theory Using Four Species of Lake Michigan Algae , 1981 .

[35]  J. Cebrian Patterns in the Fate of Production in Plant Communities , 1999, The American Naturalist.

[36]  T. Thingstad Utilization of N, P, and organic C by heterotrophic bacteria. I. Outline of a chemostat theory with a consistent concept of 'maintenance' metabolism , 1987 .

[37]  S. J. Flynn,et al.  Opening the black box of soil microbial diversity , 1999 .

[38]  J. Lennon,et al.  Source and supply of terrestrial organic matter affects aquatic microbial metabolism , 2005 .

[39]  H. Maske,et al.  Growth efficiency and respiration at different growth rates in glucose-limited chemostats with natural marine bacteria populations , 2005 .

[40]  S. Leckie,et al.  Methods of microbial community profiling and their application to forest soils , 2005 .

[41]  Michel Loreau,et al.  Plant–herbivore interactions and ecological stoichiometry: when do herbivores determine plant nutrient limitation? , 2001 .

[42]  Stefan Bertilsson,et al.  Heterotrophic Bacterial Growth Efficiency and Community Structure at Different Natural Organic Carbon Concentrations , 2003, Applied and Environmental Microbiology.

[43]  F. Celar Competition for ammonium and nitrate forms of nitrogen between some phytopathogenic and antagonistic soil fungi , 2003 .