Phototropic microbial mats are compact ecosystems containing hundreds of different organisms that capture and transform energy from the sun. While cyanobacteria are the primary producers in these systems, the exchange of nutrients and recycling of light energy among all members of the community leads to stability of these ecosystems under dynamic conditions.
The microbial mats found in extreme environments, such as the hypersaline Hot Lake in Washington State, are ideal systems for studying mechanisms of energy transformation that could have applications in enhancing efficiency and stability of engineered microbial systems.
In this study, researchers at PNNL combined metagenomics with measurements of biogeochemical gradients to elucidate for the first time the relationship between the spatial distribution of organisms and metabolic functions within the mat. Leveraging the ability to segregate and extract individual genomes from metagenomic data, their analysis revealed that such communities have adapted to their dynamic environment through metabolic flexibility and sequential energy exchange.
The research offers insights into the mechanisms of energy exchange that provide foundational understanding we need in order to manipulate microorganisms for bioenergy applications.
Phototrophic mat communities are model ecosystems for studying energy cycling and elemental transformations. Complete biogeochemical cycles including carbon and nitrogen cycling, occur over millimeter-to-centimeter scales, but until now, researchers had not examined how individual organisms capture energy and macronutrients and their subsequent flow through the community.
This study used shotgun metagenomic sequencing to reconstruct the genomes of organisms from the hypersaline microbial mat community from Hot Lake in Washington State.
The Hot Lake mats are distinct from other hypersaline environments because they develop seasonally in a largely undisturbed high magnesium sulfate environment. The unique chemistry and hydrology of this system has implications for the search of life on Mars and other planetary bodies, in addition to applications in developing alternative energy systems and high-salt industrial processes.
The Hot Lake mat has three distinct layers. Researchers were able to examine the gene distribution profile across the mat depth, and, critically, to associate important pathways for nutrient and energy transformation to specific organisms through reconstruction of genomes from metagenomics sequencing. The gene profiles suggest that metabolic flexibility and mixotrophy—organism using a mix of different sources of energy and carbon—is common in organisms from Hot Lake and is a likely explanation of microbial mat survival in such extreme conditions.
An interesting finding was the distribution of three different cyanobacteria that were layered across the sharp daytime light and oxygen gradients found in the top 3mm of the mat. These organisms were distinct from the cyanobacterial species found in other hypersaline and marine systems.
Despite differences in cyanobacterial populations, many of the bacterial genomes from the Hot Lake mat are similar to those found in other studied phototrophic mats suggesting that products provided by the cyanobacteria to the community at large are similar or the same, and thus the underlying metabolisms of biomass consumers and recyclers may be conserved across microbial mats from different environments.
“This really underscores the utility of using these unusual systems as research platforms,” said PNNL researcher and co-author Bill Nelson. “The lower complexity simplifies the research, and we still learn universal principles of microbial interactions.”
The resolution of near-complete genomes from the metagenomics data revealed the metabolic flexibility and adaptability of community members to environmental conditions like light penetration, the availability of oxygen, and the availability of metabolic substrates, which are constantly changing over the course of a day.
Organisms with partial nitrogen and sulfur metabolic pathways were widespread, suggesting extensive metabolic partnerships between organisms. This contrasts with more traditional culturing and isolation studies that have selected for microorganisms containing complete biogeochemical pathways, and highlights the advantage of using metagenomic sequencing to better explore microbial communities.
The spatial arrangement of organisms within the mat changed over a 24-hour period, indicating that in response to temporal changes in the environmental gradients (likely driven by the day-night light cycle), organisms displayed metabolic flexibility and syntrophy (the cross-feeding of species).
This “rewiring” of the networks of energy and nutrient transfer within the hypersaline mat microbial community, in addition to the metabolic flexibility of the species present, suggest energy and biogeochemical partitioning within hypersaline mats is more dynamic than previously thought.
This work was supported by the U.S. Department of Energy, Office of Biological and Environmental Research (BER), as part of BER's Genomic Science Program. A portion of the research was performed using Environmental Molecular Sciences Laboratory, a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory.
J. Mobberley, S. Lindemann, H. Bernstein, J. Moran, R. Renslow, J. Babauta, D. Hu, H. Beyenal, W. Nelson. “Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat,” FEMS Microbiology Ecology, Volume 93, Issue 4, 1 April 2017, fix028, https://doi.org/10.1093/femsec/fix028