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

Iron-Mediated Microbial Interactions with Primary Producers in Terrestrial and Aquatic Systems

Authors:

Rhona Stuart1* (stuart25@llnl.gov), Naomi Gilbert1, Nicole Coffey2, Rachel Hammer3, Ikumi Ellis2, Xavier Mayali1, Peter Weber1, Christine Hawkes3, Rene Boiteau2

Institutions:

1Physical and Life Sciences, Lawrence Livermore National Laboratory; 2University of Minnesota–Twin Cities; 3North Carolina State University

URLs:

Goals

Algal and plant systems have the unrivaled advantage of converting solar energy and carbon dioxide (CO2) into useful organic molecules. Their growth and efficiency are largely shaped by the microbial communities in and around them. The μBiospheres Science Focus Area seeks to understand phototroph-heterotroph interactions that shape productivity, robustness, the balance of resource fluxes, and the functionality of the surrounding microbiome. This team hypothesizes that different microbial associates not only have differential effects on host productivity but can change an entire system’s resource economy. This approach encompasses single cell analyses, quantitative isotope tracing of elemental exchanges, omics measurements, and multi-scale modeling to characterize microscale impacts on system-scale processes. Researchers aim to uncover cross-cutting principles that regulate these interactions and their resource allocation consequences to develop a general predictive framework for system-level impacts of microbial partnerships.

Abstract

Iron (Fe) is an essential micronutrient, and microbial Fe acquisition strategies are predictive of host health across an array of environments. Despite this, a molecular level understanding of microbial Fe acquisition influence on partnership outcomes and system-level carbon (C) flux is lacking. Here, the group examines both algal-bacterial and plant-fungal interactions in response to changes in Fe to elucidate exchange mechanisms governing these interactions.

Researchers first examined bacterial isolates that grow with model diatom Phaeodactylum tricornutum. With the Boiteau laboratory at University of Minnesota (UMN), the team grew P. tricornutum alone or in co-culture with isolates under different concentrations of Fe-dust. The group used global exometabolomic profiling to determine the diatom Fe limitation response and compounds consumed or exuded by bacteria. When P. tricornutum’s growth is limited by Fe, the algae decreases production of saturated fatty acids relative to Fe-replete conditions. Some bacteria aid in algal Fe acquisition under limitation, significantly increasing algal abundance (p<0.02). Other bacteria compete for scarce Fe resources, significantly inhibiting algal growth under low Fe dust (p<0.05). These shifts in algal growth with and without bacterial partners under low Fe were accompanied by metabolomic shifts, providing insight into molecular drivers of growth.

To understand the systems-level impacts of these Fe acquisition strategies, it is important to also examine the role of bacteria-bacteria interactions. Researchers therefore examined effects of Fe limitation in a simplified community (~30 bacterial taxa) grown with P. tricornutum as the sole organic C source. The group found that under conditions of low dissolved Fe, the bacteria:alga ratio decreases significantly and the community composition shifts. The team hypothesizes that Fe-limitation enriches for taxa that can grow under reduced Fe (e.g., siderophore secretion) and/or low organic C. To determine whether algal organic C quality as well as Fe-chelating compounds shift with Fe, the group profiled the exometabolites. Initial results suggest algal-bacterial exudation and consumption are distinct under different Fe regimes. This points to a tight coupling of Fe and C in the P. tricornutum microbiome and regulation by external factors (e.g., nutrient limitation) and host physiological state.

On the plant-fungal side, with the Hawkes laboratory at North Carolina State University, researchers isolated diverse Ascomycota fungi from switchgrass roots and grew plants with single fungal partners. The team found significant fungus-dependent variation in plant Fe content, suggesting the different fungi had distinct Fe acquisition strategies and/or host transfer mechanisms. To test this, the Boiteau laboratory conducted global metabolomic profiling of 19 fungal isolates under Fe limitation. The non-siderophore producer Trichoderma had the largest negative effect on plant Fe, while the fusarinine-producing strain Chaetomium resulted in the largest increase in plant root Fe uptake (1.8 and 2.4-fold in shoots and roots, respectively, relative to non-inoculated controls). Fungi with distinct Fe uptake and metabolic strategies differentially impact plant Fe acquisition and are likely to constrain switchgrass productivity.

In summary, the group finds that Fe has an important role in phototroph-host interactions and system productivity. By characterizing microbial Fe acquisition strategies and associated C flux, researchers aim to gain a predictive understanding of the role of Fe across a broad range of host-microbe interactions.

References

This work was performed under the auspices of the U.S. DOE at Lawrence Livermore National Laboratory (LLNL) under Contract DE-AC52- 07NA27344 and supported by the BER program’s GSP under the LLNL Biofuels Science Focus Area, FWP SCW1039 LLNL-ABS-860548.