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Systems Biology to Advance Understanding of Carbon Cycling and Other Biogeochemical Processes

 

Rationale

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 molecularscale 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.

Systems Biology Approaches

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:

  • Systems biology studies on microbes, microbial consortia, and microbe-plant interactions involved in large-scale terrestrial carbon cycling processes, with particular emphasis on moving organisms that have been determined to play key roles to experimentally tractable model organism status.
  • Determination of the role of microbial communities as key points of integration between major biogeochemical cycles (e.g., carbon, nitrogen, sulfur, and phosphorus) and how these interconnections impact the rate and magnitude of carbon cycle processes in changing ecosystems.
  • Further development of environmental omics approaches (e.g., metagenomics, metatranscriptomics, and metaproteomics) and associated data integration tools to investigate in situ microbial community functional processes involved in carbon cycling.
  • Development of omics-enabled techniques for imaging and analysis of microbial community structure and function in terrestrial environments, with particular emphasis on tools permitting high-resolution and quantitative measurements in technically challenging settings such as soils, sediments, and key interfacial environments (i.e., decaying organic material, mineral aggregates, and plant roots).

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 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.

Current BER-Funded Carbon Cycling Research

In 2013, BER solicited applications for omics-driven basic research in three areas focused on the contribution of prokaryotic and eukaryotic microbes and microbial communities to carbon cycling processes in terrestrial ecosystems:

Systems biology studies on regulatory and metabolic networks of microbes, microbial consortia, and microbe-plant interactions involved in biogeochemical cycling of carbon. Proposed studies should focus on systems biology research using model microbes or microbial consortia relevant to large-scale carbon cycling processes in terrestrial ecosystems. Model systems should be carefully chosen to facilitate development of metabolic and regulatory network models that ultimately could inform larger-scale biogeochemical models of microbial processes in the environment.

Development of omics approaches to investigate microbial community functional processes involved in carbon cycling in terrestrial ecosystems. Applications should address adapting genome-enabled techniques (e.g., metagenomics, metatranscriptomics, and metaproteomics) to interrogate relevant functional processes of microbes in terrestrial environments—either at field sites or using model micro- and mesocosms—and integrating resulting data into process understanding at the ecosystem scale. Applications are encouraged that target key microbially mediated carbon cycling processes in terrestrial systems to predict responses to shifts in temperature, carbon dioxide (CO₂) concentration, or other climate change variables.

Development of omics-enabled methods and technologies for imaging and analyzing microbially mediated carbon cycling processes in terrestrial ecosystems. New approaches are needed for high-resolution characterization of microbial community structure and function in soils and other terrestrial environments. Applications are encouraged that will enable in situ analysis of functional processes of microbial communities and characterization of physical and chemical microenvironments at interfaces between microbes and biotic or abiotic surfaces (e.g., plant roots and soil aggregates).

In addition to addressing these three focus areas, researchers also were encouraged to incorporate project elements aimed at developing data-driven systems biology applications in collaboration with the DOE Systems Biology Knowledgebase. Key points of emphasis in this area included building tools for integrating and visualizing omics data at the microbial community scale and developing methods that link dynamic regulatory and metabolic networks to higher-scale biogeochemical process understanding.

See the full listing of 2013 awards.

Related, complementary research is also being funded by DOE BER's Climate and Environmental Sciences Division (CESD), which focuses on a predictive, systems-level understanding of the fundamental science associated with climate change and DOE’s environmental challenges—both key to support the DOE mission.
For more information, contact Joe Graber, 301-903-1239.

Previous BER-Funded Carbon Cycling Research

In July 2009, BER solicited proposals for basic research on the contributions of microbes and microbial communities to carbon cycling processes in the following areas:

Systems-level studies on regulatory and metabolic networks of microbes and microbial consortia involved in biogeochemical cycling of carbon. Studies are focused on systems biology research using environmentally relevant model microbes or microbial consortia. Funded projects are examining the impacts of shifts in environmental variables—such as temperature, CO₂ concentration, and availability of water and nutrients—on microbial carbon processing. Investigators were asked to carefully model systems choose that would facilitate development of metabolic and regulatory network models that could ultimately inform larger-scale biogeochemical models of microbial processes in the environment. Interdisciplinary collaboration was encouraged to link laboratory studies of the chosen model system with environmentally relevant conditions.

Development of metatranscriptomic, metaproteomic, and other genome-enabled approaches to understand how shifts in environmental variables impact microbially mediated carbon cycling processes in terrestrial ecosystems. Research is focused on addressing the adaptation of genome-enabled techniques to the interrogation of terrestrial environments, either in situ or using model micro- or mesocosms. Funded projects are targeting key microbially mediated carbon cycling processes in terrestrial systems to predict responses to shifts in temperature, CO₂ concentration, and nutrient availability, among other things. Also encouraged were projects that use genome-enabled techniques to identify and predict the impact of potentially beneficial associations between plants and microbes or microbial communities (both prokaryotic and eukaryotic) on overall ecosystem productivity.

Development of methods and techniques for imaging and analyzing microbially mediated carbon cycling processes in terrestrial ecosystems. New approaches are needed for high-resolution characterization of microbial community structure and function in soils and other terrestrial environments. Research is focused on enabling in situ analysis of the functional processes of microbial communities and characterization of physical and chemical microenvironments at interfaces between microbes and biotic or abiotic surfaces (e.g., plant cells and soil aggregates).

See a full listing of the 2010 awards.

 

Featuring

Carbon Cycling 2013 Summary of projects awarded [10/13]


Overview: Biological Systems Research on the Role of Microbial Communities in Carbon Cycling [7/11]


Carbon Cycling and Biosequestration Report [12/08]


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