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Front. Microbiol. | doi: 10.3389/fmicb.2017.02299

From genes to ecosystems in microbiology: Modeling approaches and the importance of individuality

  • 1University of Birmingham, United Kingdom
  • 2Wageningen University & Research, Netherlands
  • 3Universitat Politecnica de Catalunya, Spain
  • 4University of California, Davis, United States
  • 5Tianjin University, China
  • 6Northeastern University, United States

Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observations have advanced to the molecular and in particular gene level. However, microbial ecology models have changed less and a current challenge is to make them utilize the knowledge and observations at the genetic level. We review published models that explicitly consider genes and make predictions at the population or ecosystem level. The models can be grouped into three general approaches, i.e., metabolic flux, gene-centric and agent-based. We describe and contrast these approaches by applying them to a hypothetical ecosystem and discuss their strengths and weaknesses. An important distinguishing feature is how variation between individual cells (individuality) is handled. In microbial ecosystems, individual heterogeneity is generated by a number of mechanisms including stochastic interactions of molecules (e.g., gene expression), stochastic and deterministic cell division asymmetry, small-scale environmental heterogeneity, and differential transport in a heterogeneous environment. This heterogeneity can then be amplified and transferred to other cell properties by several mechanisms, including nutrient uptake, metabolism and growth, cell cycle asynchronicity and the effects of age and damage. For example, stochastic gene expression may lead to heterogeneity in nutrient uptake enzyme levels, which in turn results in heterogeneity in intracellular nutrient levels. Individuality can have important ecological consequences, including division of labor, bet hedging, aging and sub-optimality. Understanding the importance of individuality and the mechanism(s) underlying it for the specific microbial system and question investigated is essential for selecting the optimal modeling strategy.

Keywords: microbial ecology, gene-centric modeling, metabolic flux modeling, Agent-based modeling, Individuality, heterogeneity, single cell

Received: 25 Jul 2017; Accepted: 07 Nov 2017.

Edited by:

Steve Lindemann, Purdue University, United States

Reviewed by:

Matthew B. Sullivan, The Ohio State University Columbus, United States
Christopher S. Henry, Argonne National Laboratory (DOE), United States  

Copyright: © 2017 Kreft, Plugge, Prats, Leveau, Zhang and Hellweger. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Ferdi L. Hellweger, Northeastern University, Boston, United States, ferdi@coe.neu.edu