Modeling bacterial utilization of dissolved organic matter : Optimization replaces Monod growth kinetics

A bioenergetic model has been developed to examine growth kinetics associated with bacterial utilization of dissolved organic matter (DOM), NH4+, and N03-. A set of 11 metabolic reactions are used to govern the incorporation, oxidation, and N remineralization of DOM and dissolved inorganic N associated with bacterial growth. For each reaction, free energies and electron transfer requirements are calculated based on the C, H, 0, and N composition of the substrates and their concentration in the environment. From these reactions, an optimization problem is constructed in which bacterial growth rate is maximized subject to constraints on energetics, electron balances, substrate uptake kinetics, and bacterial C : N ratio. The optimization approach provides more information on bacterial growth kinetics than do the Monod-type models that are typically used to describe bacterial growth. Simulations are run to examine bacterial C yield and growth rate, N remineralization or immobilization, and substrate preferences as resource concentrations and compositions are varied. Results from the model agree well with observations in the literature, which indicate that the premise of the model, that bacteria allocate resources to maximize growth rate, may be an accurate overall description of bacterial growth. Simulations indicate that bacterial growth rate and yield are strongly correlated to the oxidation state of the labile DOM, as determined from its bulk elemental composition. Furthermore, the model demonstrates that bacterial growth cannot always be explained by a single constraint (such as the C : N ratio of substrate), since several constraints are often active simultaneously and continuously change with environmental conditions. Dissolved organic matter (DOM) represents an important component of aquatic ecosystems in terms of both the size of the compartment relative to particulate organic matter (POM) and its impact on the functioning of microbial food webs. Consequently, many descriptive and experimental studies have been conducted to characterize the composition of DOM, examine its production and utilization, understand its impact on microbial dynamics, and determine the extent to which it supports higher trophic levels. The results of these studies have been incorporated to various extents in both simple bacterial growth models and more complete food web models that examine DOM utilization. These models are based almost Acknowledgments We are indebted to Ed Rastetter and Mat Williams for their comments during the preparation of this manuscript. We also appreciate the constructive criticism of David Kirchman and two anonymous reviewers. This manuscript was supported by grants from the Lakian Foundation, the National Science Foundation Land Margin Ecosystems Research program (OCE 921446 l), and the DOE Ocean Margins Program (92-R6 1438). exclusively on Monod-type growth expressions in which bacterial C yield (mol bacterial C/m01 C consumed, also called bacterial growth efficiency) and maximum specific growth rate are fixed, and N uptake or excretion is determined by C and N mass balances. Although these Monod-type models have been quite useful for improving our understanding of microbial food webs, they prove difficult to use for detailed studies of bacterial DOM processing because they do not account for the variable energy content and oxidation state of DOM. Here we present a new, bioenergetically based model for describing bacterial utilization of DOM based on growth rate optimization subject to constraints on energy, redox reactions, substrate uptake kinetics, and the C : N ratio of bacteria. It is well known that bacteria are primarily responsible for the processing of DOM in aquatic environments (Wright and Hobbie 1966; Azam and Hodson 1977) and that the efficiency with which bacteria utilize dissolved organic C (DOC) is an important factor governing the flow of C and energy through the microbial food web that leads to higher trophic levels (Azam et al. 1983; Duck101 et al. 1986; Sherr et al. 1987; Turner and Roff 1993). TJ extent to which dissolved organic N (DON) is remir