Risk and Return: The economics of a photosynthetic cell

Today me and my co-authors published a paper in Cell Reports that is the result of a roughly two-year adventure into the economics of cyanobacteria. Now you wonder, what are cyanobacteria and why have they anything to do with economics? These questions evolve around a concept that has recently gained more attention, namely that the behavior of cells is governed by the availability of goods, and the need to make the best out of them when they’re limited. Let’s take a brief walk through the main ideas of the paper.

Every microbe has its niche

Every microbial cell has its environmental niche. The famous Escherichia coli lives in our guts, lactic acid bacteria thrive in dairy products (or where they came from), and the cyanobacteria’s realm is every water body from the sea to the sweet water pond. But they are not alone. All microbial cells have to compete with other cells and other species for resources. We can safely assume that, apart from occasional feasting events, resources are scarce. In this competitive environment cells that harvest and utilize these resources in the best way have the best chance of producing offspring. This sounds trivial but some of the behavior that microbes show is somewhat less intuitive.

How cells respond to limitation

What is already known for several decades is that model microbes like E. coli adjust their investment in enzymes (and other proteins) depending on the substrate concentration (that is, how much food they have). As a simple example, a cell with abundant substrate will invest more resources in making ribosomes which are the factories inside the cell that make more proteins, meaning more biomass, and faster growth. The relationship between ribosome abundance and growth rate is even strictly linear! Now comes the non-intuitive part: The more substrate the cells have around them, the less they invest in harvesting it. This is like attending an all-you-can-eat-buffet but just picking a sandwich from the nearest table. The underlying reason is that the size of a microbial cell is limited by biophysical laws (like diffusion), making it impractical to simply expand and accommodate all possible enzymes. Instead, cells reduce the costs for substrate assimilation and invest more in converting substrates to biomass equals offspring.

Cyanobacteria have dedicated proteins to harvest light (LHC) and CO2 (CBM). The ribosomes (RIB) in turn are responsible to turn these resources into new proteins (65% of cell biomass). Protein allocation changes under the transition from high to low light.

Now what have cyanobacteria to do with that?

Cyanobacteria are special. They (usually) don’t eat sugar but make all biomass from CO2 and the energy contained in sunlight. Just like plants do, and cyanobacteria are just as green as plants, only smaller and simpler in their architecture. The difference to well-studied bugs like E. coli is that cyanobacteria need to invest many more resources in collecting CO2 and energy from light, using for instance large dedicated antennae to scavenge photons. Nobody knows if such an autotrophic (without sugar and the like) living cell balances the demands for growth, light and CO2 assimilation in a similar way as E. coli does when growing on sugars. We filled this gap by growing cyanobacteria under highly controlled conditions in photo-bioreactors and measuring the overwhelming majority of its proteins (around 90% by mass).

A figure from the paper showing the linear increase or decrease of major functional protein groups (A). The response to light (red symbols) and CO2 limitation (blue symbols) is different. (B) shows the biggest players in terms of protein mass and (C,D) a show maps of the proteome under the two limitations.

The economics come into play

We determined the protein composition of cells either under increasing light or CO2 concentration and found that the abundance of important groups changed linearly with growth rate. For example, the cells invest ever more resources in collecting light energy when it’s darker; As a consequence, there is less space for ribosomes, resulting in overall lower growth rate. We also found that the response to light limitation is stronger than the response to CO2, and that antenna proteins bind the most cellular resources of all. And finally, we compared the experimental findings with predictions from a mathematical resource allocation model. This model suggests that resource allocation largely follows an optimal scheme, but that cells deviate from optimality under some conditions (to be investigated). What can we learn from all that? Generally, now we know better how photosynthetic cells cope with limitation. The results also confirm previous observations on resource allocation in other bacteria and make this strategy seem universal.