Integration of systems biology and ecology: A mesocosm-scale study designed to span the gene-ecosystem continuum

Ecological systems are characteristically hierarchical and there is constant interplay between multiple levels of biological organization. This interplay extends from events that happen rapidly at the level of cells to events that operate more slowly at the level of populations and communities. Although studies that span this gene to ecosystem continuum can provide a unique and hopefully informative perspective on the response of organisms to their environment, few studies have identified explicit linkages from genes to ecosystems. Therefore, we initiated the Hierarchical Experimental Responses at Macromolecular to Ecosystem Scales (HERMES) project to explore how mechanisms at one level of biological organization can be understood in terms of consequences at a different level of organization. Our approach involves growing wild-type and mutant Arabidopsis plants at ambient and elevated carbon dioxide concentration in simplified, yet highly-controlled model ecosystems. Wild type plants and mutants that lack an important gene for nitrate reductase activity are being grown in competitive mixtures. Changes in the relative abundance of plants are tracked over multiple generations, while a suite of measurements characterize changes in global gene expression, enzymes, metabolites, and physiology, and relate these effects to changes in biomass production, flowering, seed production, and germination and subsequent changes in population, community, and ecosystem-scale processes. Now in their fourth generation, wild-type and mutant plants show distinct patterns of behavior both with respect to each other and to imposed carbon dioxide treatments. We discuss these differences in terms of systems biology, plant growth and development, reproductive biology, and carbon and nitrogen cycling. A unifying hypothesis to explain our observations is presented.