Microorganisms: Life on the energetic edge

Microorganisms
Fig. 1 Cellular energy balance. The figure shows a bacterial cell that generates energy by coupling the oxidation of an organic compound (here, lactate) to the reduction of nitrate in a process called dissimilatory nitrate reduction to ammonium, or DNRA. The energy is used for new biomass growth (anabolism) and maintenance. Some energy is also lost to the environment as heat. The symbol G stands for Gibbs energy, which is the fraction of the total energy that can be transformed into work; ΔGcatabolism is the Gibbs energy released during DNRA. The quantitative description of the cellular energy balance forms the basis of the theory of bioenergetics.

Just a spoonful of soil harbours more microbes than there are people on Earth and one litre of seawater may contain more than a billion bacteria. Microorganisms make up most of the Earth’s biomass and are the foundation of all terrestrial and aquatic ecosystems. Single-celled organisms regulate the processes that underpin the biogeochemical cycling of carbon, macronutrients (e.g., phosphorus, nitrogen, silicon and sulphur) and many trace elements, with far-reaching consequences for soil fertility, climate, and water quality.

Microorganisms play key roles in waste management and environmental remediation. They are also among the main producers of greenhouse gases including carbon dioxide, methane, and nitrous oxide, hence closely coupling microbial activity to the Earth’s climate system.

Since the mid-1990s, our ability to decipher the structure and functional diversity of natural microbial communities has grown tremendously through the application of advanced molecular biology techniques. However, the representation of complex microbial communities in environmental models, such as reactive transport models, remains rudimentary. In most cases, microorganisms are treated as simple catalysts of chemical reactions. This limits the ability for models to predict when and where a given group of microbes will thrive. A major research thrust in the Ecohydrology Research Group (ERG) at the University of Waterloo is to overcome this limitation through the application of bioenergetics.

Explaining bioenergetics

Whether a tree, an elephant, or a bacterial cell, for all life forms the ability to turn energy into biological work is essential. The largest source of energy fuelling the biosphere is sunlight through the process of photosynthesis carried out by plants, algae, and certain bacteria. Most single-celled organisms, however, must utilise chemical compounds (referred to as substrates) as their source of energy. Our research focuses on these so-called chemotrophic microorganisms.

In microbial bioenergetics, thermodynamic principles are applied to quantitatively describe energy transformation and utilisation by microorganisms. The energy transformation begins by identifying the energy-yielding (or catabolic) reactions used by the cells to generate energy from chemical substrates extracted from their surroundings. For example, many aerobic microorganisms rely on the energy obtained from the breakdown of extracellular organic molecules to carbon dioxide (CO2) by molecular oxygen (O2). The catabolic energy allows the cells to produce new biomass and perform maintenance. It also allows the cells to perform other functions, such as acquiring essential nutrient elements or neutralizing toxins, while some energy is dissipated as heat (Figure 1).

The way cells partition energy provides bioenergetic constraints that can be incorporated into kinetic models. Kinetic models compute the rates at which microorganisms consume chemical substrates (for example, carbohydrates and O2), grow new biomass, and release reaction products (for example, CO2). In principle, a bioenergetics-informed kinetic model can simultaneously predict the changes in the microbial community structure and the accompanying chemical changes of the environment in which the microbes live.

Microbial bioenergetics matter

The application of bioenergetics is well-established in industrial biotechnology. One example of the current application of bioenergetics is in waste water treatment. However, it is rarely applied when modelling microbially mediated chemical transformations taking place in natural and human-modified ecosystems, such as deep lakes, ocean sediments, aquifers, constructed wetlands or mine tailings. Particularly in deeper subsurface environments, the energy supply that sustains chemotrophic communities is typically quite low. This means that these communities survive at the energetic edge. Much of our work on bioenergetics centres on the development of quantitative models that describe the functioning of microbial communities under energy limiting conditions, and the consequences for biogeochemical cycles at local to global scales (Figure 1).

Bioenergetics research within the Ecohydrology Research Group follows a three-pronged approach (Figure 2): 1) incorporating theoretical principles from bioenergetics into kinetic models for microbial reaction rates; 2) verifying these models using laboratory or field data, and 3) applying the models to predict the fate and transport of nutrients, contaminants and greenhouse gases in environmental systems.

Microorganisms
Fig. 2 ERG’s integrated approach to bioenergetics: from theory, via experimental verification, to environmental modeling.

Gibbs Energy Dynamic Yield Method – GEDYM

One example of a recent theoretical development is GEDYM, a bioenergetics-based approach to calculate microbial growth yields (Y) under variable physical and chemical conditions. The growth yield corresponds to the fraction of the catabolic energy that microbial cells invest in growth. It provides a measure of the efficiency with which microbes convert resources into new biomass. GEDYM therefore enables to dynamically couple microbial chemical activity to changes in microbial community composition. This marks a major advance, because, until GEDYM, reactive transport models usually assigned fixed Y values to different microbial groups with no flexibility to adjust the values in response to changes in their chemical environment. Additionally, existing experimental data confirm that GEDYM performs better than other methods when predicting growth yields for microorganisms that depend on low energy yielding catabolic reactions, such as methane producing microbes.

Who does what where?

Most subsurface environments are chemically complex and may be highly changeable in space and time. Key challenges are therefore to determine where and when a microbial group will be active, whether the cells will use an organic or inorganic energy substrate, and what metabolic waste products they will release into their surroundings. To answer these questions, we developed an optimization approach which deduces the combination of microbial metabolisms that makes the best use of the available energy supply. For example, we are applying this approach to delineate under what conditions it becomes advantageous for a soil microbial community to start utilizing CO2 as a carbon source for biomass growth, rather than only relying on organic compounds. Answering this question is significant, because what carbon sources are consumed impacts a soil’s overall carbon budget and, ultimately, determines how much CO2 the soil emits to the atmosphere. The optimization approach is particularly useful for microbial reaction processes that cannot be reproduced easily in the laboratory. For example, when a process is very slow or because there are no cultural microbes to perform the process, or for processes that take place in environments that are difficult to access, such as a deep aquifer or oil reservoir.

In another study, we are assessing the environmental controls on the microbial reactions that modulate methane (CH4) production in subsurface ecosystems. The results reveal a very strong effect of temperature on the CH4 yielding reaction pathways, which in turn have quite distinct effects on the mix of CH4 and CO2 that is generated. The latter is important, because CH4 is a much stronger greenhouse gas than CO2. In the context of ongoing global warming, this implies that the way we view and represent the response of CH4 and CO2 emissions to changes in subsurface thermal regimes in global scale Earth System Models very much depends on how well we understand the microscale bioenergetic constraints on methane producing microbes.

What’s next?

The field of environmental microbial bioenergetics is still wide open.  The theoretical framework we have begun to develop within ERG can be further expanded to account for other limiting factors, for instance the availability of essential nutrient elements, or by including more general representations of energy allocation to non-growth processes, such as detoxification and the temporary intracellular storage of energy reserves by microorganisms.

Read more

Smeaton, Christina M., and Van Cappellen, Philippe. “Gibbs Energy Dynamic Yield Method (GEDYM): Predicting microbial growth yields under energy-limiting conditions.” Geochimica et Cosmochimica Acta 241, pp. 1-16 (2018).

https://www.sciencedirect.com/science/article/pii/S0016703718304630?via%3Dihub

microorganisms

Special Report Author Details
Author: Christina Smeaton and Philippe Van Cappellen
Organisation: Ecohydrology Research Group
Telephone: +1-519-888-4567 ext. 31319
Email: christina.smeaton@uwaterloo.ca
Email: pvc@uwaterloo.ca
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