Abstract

Trait-based microbial models show clear promise as tools to represent the diversity and activity of microorganisms across ecosystem gradients. These models parameterize specific traits that determine the relative fitness of an “organism” in a given environment, and represent the complexity of biological systems across temporal and spatial scales. In this study we introduce a microbial community trait-based modeling framework (MicroTrait) focused on nitrification (MicroTrait-N) that represents the ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) using traits related to enzyme kinetics and physiological properties. We used this model to predict nitrifier diversity, ammonia (NH3) oxidation rates, and nitrous oxide (N2O) production across pH, temperature, and substrate gradients. Predicted nitrifier diversity was predominantly determined by temperature and substrate availability, the latter was strongly influenced by pH. The model predicted that transient N2O production rates are maximized by a decoupling of the AOB and NOB communities, resulting in an accumulation and detoxification of nitrite to N2O by AOB. However, cumulative N2O production (over 6 month simulations) is maximized in a system where the relationship between AOB and NOB is maintained. When the reactions uncouple, the AOB become unstable and biomass declines rapidly, resulting in decreased NH3 oxidation and N2O production. We evaluated this model against site level chemical datasets from the interior of Alaska and accurately simulated NH3 oxidation rates and the relative ratio of AOA:AOB biomass. The predicted community structure and activity indicate (a) parameterization of a small number of traits may be sufficient to broadly characterize nitrifying community structure and (b) changing decadal trends in climate and edaphic conditions could impact nitrification rates in ways that are not captured by extant biogeochemical models.

Highlights

  • Understanding the interaction between ecology and biogeochemistry is an important frontier in environmental microbiology

  • EMERGENT COMMUNITY ECOSYSTEM MODEL DESCRIPTION (MICROTRAIT-N) MicroTrait-N resolves intra-functional group diversity of the nitrifier populations (AOB, ammonia-oxidizing archaea (AOA), nitrite-oxidizing bacteria (NOB)) by parameterizing multiple guilds spanning a range in the trait-space (Figure 1)

  • We performed several types of simulations investigating the role of pH, temperature, decoupling nitrite, and ammonia oxidation, and pulsed NH3 inputs, by: (1) using the mean value of each trait; (2) performing Monte Carlo (MC) simulations to account for intra-guild diversity; and (3) running the model in equilibrium and dynamic steady state cycle modes to characterize the impact of temporal forcing variation on predicted emergent microbial community structure

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Summary

Introduction

Understanding the interaction between ecology and biogeochemistry is an important frontier in environmental microbiology. The theoretical background to expand numerical approaches in environmental microbiology could well follow the trait-based approach implemented in models of marine autotrophic phytoplankton (Litchman and Klausmeier, 2008; Follows and Dutkiewicz, 2011). These models have been shown to be valuable tools for understanding how communities assemble (Follows et al, 2007; Litchman et al, 2007), how they change over time (Litchman and Klausmeier, 2006), and the interdependencies between community dynamics and biogeochemistry (Dutkiewicz et al, 2009)

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