MIM: A thermodynamic theory of microbiome assembly, adaptation and evolution evaluated using modular microbial environments

Across Earth’s ecosystems, microbes adapt and form communities (microbiomes) across gradients of energy and resource richness. Like the machines and electrical circuits we engineer, power and efficiency are key features that also determine the competitiveness of microbes in communities. Over evolutionary time, microbes have optimized their own molecular machines to convert available energy with high efficiency, minimizing the loss of waste energy as heat.

Microbes have a range of strategies, reflecting the balance between the rate of new cell production (power), and its efficiency (yield), while also dealing with various costs of survival that reduce yield. This research project will test the hypothesis that microbiomes, assemble from individual members to form communities that also optimize power while increasing efficiency.

This principle of power and efficiency optimization may apply generally across different levels of biological organization from proteins to ecosystems. Researchers will study microbiomes from soils and the human gut as model systems to test this idea. They will develop a new experimental platform, involving multiple compartments to control how microbiomes interact, with integrated nanotechnology sensors to measure microbial efficiency as heat output, plus advanced microscopy to measure yield as microbes grow.

This work will test if information stored in microbial genomes can predict their power-yield strategies, and if aspects of microbiome diversity can be related to efficiency, developing a predictive modeling framework. If this fundamental thermodynamic theory can explain patterns in biological organization from cells to communities, it will provide an important new framework to predict how biology will respond to future conditions on Earth.

Broader impacts include involving community college students in the research, in addition to graduate and postdoctoral students. Outreach activities consist of developing scientific videos for a storytelling platform, which would be available to the general public.

Microbes, like all living organisms, maintain the order of life through the creation of entropy. They exist in open, non-equilibrium thermodynamic systems, across gradients of free-energy that fuel the formation and maintenance of structures (proteins, cells, communities) that enhance exergy flow, while attempting to minimize dissipation of waste heat – enhancing overall entropy production in the process.

The assembly and succession of microbial communities are driven by flows of exergy, and it is the trade-off between maximum power and minimum heat dissipation that regulate yield (i.e. efficiency). This trade-off towards the production of entropy is a fundamental thermodynamic principle. As a biological optimization function, the optimization of power and yield aligns thermodynamics and evolution through natural selection, in that constraints such as resource availability or stress, modulate the fitness of an organism depending on the placement of their power:yield strategy across a Pareto optimal curve.

How these trade-offs manifest at the community scale has not been empirically tested. This research will test this by (1) developing a novel integrated nanocalorimetry-microfluidics platform to control gradients of resources and stress, simultaneously quantifying power, yield and entropy production in an open system; (2) performing a series of manipulative experiments to evaluate how properties of microorganisms and microbiomes relate to power, yield and entropy production and bio(geo)chemical outputs, and (3) develop simulation tools based on the thermodynamics of power-yield trade-offs to predict the emergence of microbiome function and composition.

This thermodynamic theory is applicable to all living organisms, with the outcomes being generalizable beyond microbiome sciences. Co-funding for this award was provided by the Division of Materials Research.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.