Researchers have tracked the genomic composition of microbes in thawing permafrost to determine which had the greatest impact on releases of carbon dioxide and methane into the atmosphere
[Environmental Molecular Sciences Laboratory]
The global carbon cycle plays a central role in regulating atmospheric carbon dioxide levels and Earth's climate, but knowledge of the biological processes operating at the most foundational level of the carbon cycle remains limited. These processes are intimately linked to higher-scale biogeochemical processes and form key linkages between global carbon, nitrogen, and water cycles. Even minor changes in the rate and magnitude of biological carbon cycling can have immense impacts on whether ecosystems will capture, store, or release carbon. Developing a more sophisticated and quantitative understanding of molecular-scale processes that drive the carbon cycle represents a major challenge, but this understanding is critical for predicting impacts of global climate change.
The carbon cycle is heavily dependent on microbial communities that decompose or transform organic material in the environment. Massive amounts of organic carbon currently are stored in ecosystems (e.g., the soils of forests, grasslands, and permafrosts), and microbes are known to play key roles in determining the longevity and stability of this carbon and whether or not it is released into the atmosphere as carbon dioxide or methane, both greenhouse gases, under any given set of environmental variables. However, large uncertainties remain regarding the nature and magnitude of carbon cycle processes performed by environmental microbes; critical knowledge gaps in this area have proven difficult to address given the limited understanding of key groups of organisms and significant technical difficulties in characterizing microbial community functional processes in soil environments. Microbially mediated processes are only minimally represented in most higher-scale carbon cycle models, a factor contributing to uncertainties and limiting predictive capabilities.
Consequently, there is a critical need to advance understanding of the systems biology properties of microbes performing key carbon cycle processes and develop new approaches to link the structural and functional characterization of microbial communities with quantitative measurements of carbon cycle processes.
Understanding and predicting processes of the global carbon cycle require bold new research approaches aimed at linking global-scale climate phenomena; biogeochemical processes of ecosystems; and functional activities encoded in the genomes of microbes, plants, and biological communities. This goal presents a formidable challenge, but emerging systems biology research approaches provide new opportunities to bridge the knowledge gap between molecular- and global-scale phenomena. Systems-level research emphasizes studies on the underlying principles of intact, complex systems and facilitates scaling of concepts and data across multiple levels of biological organization. Applying this approach to the global carbon cycle will require multifaceted, but highly integrated research that incorporates experimentation on model organisms and systems, collection of observational data on communities and ecosystems, and mechanistic modeling of processes ranging from metabolic to global scales.
As described previously, the Genomic Science program approach to systems biology—coupling modeling and simulation with experiment and theory—aims to define the organizing principles that control the functional capabilities of organisms. Researchers have made significant strides in extending these approaches beyond well-characterized model organisms such as Escherichia coli and applying them to poorly understood microbes that only recently may have been brought into cultivation from environments of interest. Recent efforts have seen a rapid acceleration in researchers' ability to characterize newly isolated microbes, develop genetic tools for experimental manipulation, and build predictive models of metabolic and regulatory processes. Applying these approaches to key carbon cycling microbes such as methane-consuming bacteria, methane-producing archaea, and syntrophic consortia of organisms responsible for processes that cannot be performed by independent microbes has yielded surprising discoveries of previously unknown capabilities that have important implications for understanding microbes' roles in environmental processes.
To advance this understanding, researchers must move beyond single-organism studies and extend systems biology approaches to more complex microbial communities, the influence of changing environmental variables on functional attributes, and relationships with associated plant communities. Increasingly sophisticated approaches for metagenomics, metatranscriptomics, and metaproteomics (as well as computational tools for associated data analysis and integration) offer new methods for investigating the metabolisms and lifestyles of microbial communities, including uncultivated organisms from environmental samples. Continued development of "meta-omic" research techniques, especially when coupled with approaches permitting analysis and visualization of molecular-scale functional processes, not only will help capture the functional potential encoded in genomes, but also will enable new approaches for qualitatively and quantitatively measuring active processes in the environment. The knowledge gained via these approaches will expand understanding of molecular-scale carbon cycling processes and their sensitivities to shifting environmental variables, and that knowledge (and, where appropriate, derived data) can be scaled to help refine understanding of processes at higher levels of organization.
The response of ecosystems to environmental change depends on the collective responses of many types of organisms whose functions are encoded in genomes. Although linking directly from genomes to global phenomena is not necessarily practical for terrestrial systems with current approaches, many connections at intermediate scales are viable with integrated application of new systems biology approaches and powerful analytical technologies and modeling techniques aimed at linking physiological and ecosystem-level process understanding. By adapting genome-enabled techniques to the investigation of microbial systems (either via in situ observations at field sites or by using micro- or mesocosms for manipulative experiments), this research will pave the way to more quantitative, community-scale systems biology approaches that can inform larger-scale biogeochemical models of microbial processes in the environment.
Specific knowledge gaps in carbon cycling processes that are being addressed by the Genomic Science program include:
Gaining a mechanistic understanding of the impact microbial communities have on carbon cycling enables more accurate predictions of the feedbacks between the terrestrial environment and the atmosphere under a variety of changing climate scenarios.
In addition to their impact on carbon cycling, microorganisms can profoundly affect the biogeochemical characteristics of soils and sediments, thereby influencing the mobility and fate of materials in the environment. Although numerous processes influence the transport of metals, contaminants, and nutrients, microbiological activity is arguably the least-understood component of these processes. Microbial communities, through their interactions with each other and with geologic materials, play a role in modifying the local geochemical environment, thereby impacting the chemical form and mobility of materials in subsurface and surface environments, particularly at key intersections between the two (thus contributing to broader biogeochemical cycles).
A key to successfully understanding these systems will lie in establishing the link between biological processes performed by microbial communities and site-specific geochemistry. Many systems biology-enabled techniques and approaches described here and on our Sustainability Research page also are applicable to this DOE mission challenge for the Genomic Science program, and were in many cases initially developed for studies of subsurface microbial communities.
Improving the mechanistic understanding of key biogeochemical processes mediated by microbial communities facilitates the development of more predictive field-scale models of environmental processes. Microbial processes often are abstracted as static descriptions of individual enzymatic processes, yet the influence of community composition, growth, stress, and nutrient limitation (among many others) can greatly affect activity across spatial and temporal scales. New systems biology-enabled understanding offers the ability to describe how individual microbes and microbial communities function in response to changing environmental parameters and vice versa. Furthermore, the integration of systems biology and modeling approaches that link omics-derived data on microbial community structure and function with data from biogeochemical and environmental measurements will provide new mechanistic ways to more accurately describe and predict the dynamic interplay between microbes and their environment.
The Genomic Science program will continue to facilitate detailed discovery and investigation of microbes and microbial ecosystems that play roles in the fate and transport of metals, contaminants, and nutrients in subsurface environments. These studies will expand knowledge about structure, function, metabolic activity, and the dynamic nature of microbial communities and their interaction with the geochemical environment. Research on microbial community structure and function in these environments also provides opportunities to further develop community-scale systems biology tools linked to biogeochemical process understanding and pose more foundational questions relating to ecological theories and their applicability to microbial communities.