Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Understanding Microbial Invasion Biology from Laboratory-to-Field for Secure Ecosystem Engineering and Design

Authors:

Paul E. Abraham* (abrahampe@ornl.gov), Melissa Cregger, Alyssa Carrell, Dana Carper, Aaron Onufrak, Sameer Mudbhari, Emily Smith, Tomas Rush, Joanna Tannous, Joshua Michener

Institutions:

Biosciences Division, Oak Ridge National Laboratory

URLs:

Goals

The Secure Ecosystem Engineering and Design (SEED) Science Focus Area (SFA), led by Oak Ridge National Laboratory, combines unique resources and expertise in the biochemistry, genetics, and ecology of plant-microbe interactions with new approaches for analysis and manipulation of complex biological systems. The long-term objective is to develop a foundational understanding of how non-native microorganisms establish, spread, and impact ecosystems critical to U.S. DOE missions. This knowledge will guide biosystems design for ecosystem engineering while providing the baseline understanding needed for risk assessment and decision-making.

Abstract

The deliberate introduction of plants or microbes into new environments will be necessary to address national and global energy and environmental challenges. However, scientists currently lack the knowledge and tools necessary to successfully predict and introduce beneficial alterations, prevent undesired modifications, or predict the risks of proposed ecosystem engineering efforts.

A promising strategy for ecosystem engineering is the deliberate introduction of microbes to produce a specific effect on ecosystem function (Figure 1). At the same time, the anthropogenic-assisted movement of microbes and changes in climate are accelerating the emergence of non-native pathogens in resident communities. Regardless of the source, biosystems design strategies must accommodate and encompass the dynamic ecological and evolutionary factors that determine the outcome of natural and engineered invasions into ecosystems. Accounting for these barriers and their dynamics will enable new engineering approaches to safely manipulate the introduction of genes, pathways, and microbes into ecosystems to solve critical environmental challenges while limiting undesired community perturbations.

For ecosystem engineering using plant growth-promoting bacteria, the project has identified several nonmodel strains of Bacillus as testbeds for secure biodesign and genome engineering. While Bacillus species are abundant in soils and plant tissues and are common components of commercially available biological control products, there is a growing concern that the deliberate introduction of microbes into the environment will have unintended consequences on ecosystem health. Additionally, the mechanisms underlying the establishment and impact of introduced microbes for ecosystem engineering on plant and ecosystem health are not well understood. Therefore, the team has assessed the establishment and persistence of several Bacillus spp. across a series of laboratory-to-field experiments. For these experiments, researchers have benchmarked the persistence of these nonmodel Bacillus spp. in the soil microbiomes of Populus and quantified their impact on the host and resident microbiomes.

Furthermore, there is a growing concern that the anthropogenic movement of plants and their associated microbes will accelerate the emergence of novel pathogens. Microbial functions are notoriously context dependent and, with increasing movement of microbes and changes in climate, organisms are likely to transition from mutualist to pathogen with increased frequency. One such example is the fungal pathogen Sphaerulina musiva which following the human translocation of Populus across North America, spread from its original host, Populus deltoides, to novel hosts including Populus balsamifera and the DOE-flagship species Populus trichocarpa. In its new hosts, S. musiva induces fatal stem cankers in natural and managed settings that can greatly inhibit plant production. As a result, researchers have also assessed the effects of S. musiva establishment on host plants and their associated microbial communities in laboratory-to-field experiments.

Given the commercial applications of Bacillus spp. as a biofungicide, the team has tested the interactions between nonmodel Bacillus strains against several natural isolates of S. musiva. This characterization has uncovered a range of inhibitory strengths and varying tolerances for Bacillus and S. musiva, respectively. Using these results, researchers are developing a high-throughput image-based method paired with metabolomics to understand the genetic and chemical diversity for biocontrol.

Collectively, obtaining information on the direct or indirect mechanisms that control microbial-based biocontrol targeting fungal pathogens can help improve biodesign strategies aiming to increase Populus productivity and sustainability.

Image

Four trees with roots and microbial communities in the ground. Microbial invaders are prevented from entering by locks unless they have traits which act as keys.

Figure 1. Ecosystem engineering to promote or limit microbial invasions. Natural microbial communities (black) face many potential microbial invaders (blue, green, magenta, and yellow). A successful invader must sequentially establish, spread, and produce a functional impact. Invaders have different traits (keys) that potentially allow them to proceed through barriers (locks) at each stage. By manipulating the invader (e.g., providing keys to the engineered blue strain), plant, or ecosystem (e.g., changing the locks at a given stage), an ecosystem engineer can control the outcome of these potential invasions. In this example, the engineered strain (blue) has the necessary traits to successfully deliver its payload and improve tree health while the undesired invaders (green, magenta, and yellow) are blocked.

Funding Information

The SEED SFA is sponsored by the GSP, U.S DOE, Office of Science, BER program, under FWP ERKPA17. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the U.S. DOE under contract no. DE-AC05-00OR45678.