U.S. Department of Energy

Pacific Northwest National Laboratory

Microbial Partnerships and the Genes that Underpin Interspecies Metabolite Exchange

A microbially coupled consortium.

The Science                      

In nature, very small communities of microorganisms are present in very large numbers, and therefore mediate key biogeochemical and ecological processes on a global scale. For instance, both terrestrial and aquatic ecosystems shape Earth’s climate via microbial biogeochemical cycling. (One dramatic example is the “Great Oxygenation Event” about 2.3 billion years ago, when microbial photosynthesis  introduced Ointo the Earth’s atmosphere.) For scientists it is important to understand the effect microbes have on each other and to understand the genome-encoded mechanisms by which they exchange resources such as reduced carbon, organic nitrogen, and vitamins. A new paper from researchers at the Pacific Northwest National Laboratory (PNNL) constructed a model two-species consortium to infer and test specific interspecies interactions, observed during changing environmental constraints and growth kinetics.

The Impact

Some of the observed behaviors of this novel multi-species model relate to the most foundational functions of life, such as carbon and energy acquisition. They represent putative principles in metabolic coupling between photoautotrophic primary producers and the heterotrophs that depend on them for sustenance. The paper’s chief result is evidence of indirect interspecies regulation. The study’s outcomes can be generalized and will result in a better understanding of globally ubiquitous phototroph-heterotroph interactions.

Summary

The mechanisms by which microbes interact in functionally diverse communities underpin the planet’s biogeochemical and ecological processes, yet these interspecies relationships remain poorly understood. In nature, community-level microbial responses are a function of all the species present, even those in low abundance. But natural communities are structurally and functionally complex, with interactions too entangled for researchers to observe the behavior of specific microbial species. Hence the need to infer general principles of interspecies microbial interaction by observing a model consortium grown in controlled laboratory environments. The new study by PNNL lead author Hans Bernstein and 11 co-contributors describes a model microbial consortium that infers how microbial partnerships lead to the expression of genes that encode for the synthesis and exchange of resources relevant to almost all food-webs and biogeochemical cycles. To assemble the model consortium researchers employed two well-annotated microorganisms isolated from geothermal hot springs: a phototrophic cyanobacterium and primary producer (Thermosynechococcus elongatusBP-1) in partnership with an aerobic heterotroph (Meiothermus ruberstrain A), which depends on the cyanobacterium for organic carbon, oxygen, reduced nitrogen and essential co-factors (vitamins). 

The researchers were able to couple global transcriptomic measurements to the environmental factors used to control the consortium’s growth and energy acquisition rates. They compared the results obtained from this binary consortium to a cyanobacterial monoculture control. That comparison allowed the researchers to determine which transcriptional and physiological responses were caused by interspecies partnership over a dynamic range of light and oxygen conditions. The results revealed mechanisms that enable both interspecies metabolic coupling and acclimation to partnership. The mechanisms support the hypothesis that gene expression (with its resulting changes in microbial physiology) is indirectly regulated by distinct partnerships between species.

The observed heterotrophic partnership between a producer and a consumer, among other things, increased the efficiency of biomass production (a measure of growth per unit of energy acquired) and improved resistance to oxidative stress (from high levels of dissolved oxygen). Moreover, both species underwent physiological changes induced by their partnership, which the authors used to infer specific interactions prompted by synthesis and the interspecies exchange of resources. For one, the cyanobacterium responded to heterotrophic partnership by altering the expression of core metabolic genes linked to photosynthesis, carbon uptake, and fixation, vitamin synthesis, and the scavenging of reactive oxygen species.

The study sheds light on how a cyanobacterial primary producer acclimates to a heterotrophic partnership by modulating the expression of key metabolic genes. In addition, the study shows that heterotrophic bacteria can indirectly regulate the physiology of photoautotrophic partners. The authors say the functions they describe could represent generalizable principles of phototroph-heterotroph interactions, which are ubiquitous in globally consequential natural microbial communities.

Funding

This research was supported by the U.S. Department of Energy Office of Biological and Environmental Research (BER) Genomic Science Program and is a contribution of the Fundamental Scientific Focus Area.

Publications

Hans C. Bernstein, et al., “Indirect interspecies regulation: Transcriptional and physiological responses of a cyanobacterium to heterotrophic partnership.” mSystems, 2:e00181-16.

DOI:10.1128/mSystems.00181-16

Date: 
March 2017
| Pacific Northwest National Laboratory