Marine microbiology

Research on SAR11

What is the most abundant group of bacteria in the world? The first bacteria to pop into your mind are probably household names like E. coli or Bacillus that have been studied in labs the world over for decades. Actually, the most abundant group of bacteria in the world are the unassuming microbes from the group called SAR11, so called because the first described DNA sequence from this group was from the Sargasso Sea (thus SAR) and was the 11th one identified. These microbes are very small (cell volume of 0.04 cubic micrometers; you could fit 2x10^21 in a teaspoon), comma-shaped, either pink or white (depending on what part of the world you're in), ubiquitous (from Antarctic oceans to tropical, coastal to open ocean), have very small genomes (1.3 mbp; one of the smallest of any free-living organisms), and are very abundant (about a million in every drop of seawater, mostly at the surface of the ocean). 

My PhD research focused on the physiology and metabolism of these unique microorganisms using culture-based experiments. I addressed two of the big unanswered questions about SAR11: Why are SAR11 cells so abundant? How are they able to be so successful in the ocean despite having a very small genome? 

To answer the first question, I tested the hypothesis that SAR11 cells are very efficient at transporting metabolites from the surrounding seawater despite very low environmental concentrations. I used radioactively-labeled compounds to measure the uptake kinetics of a common metabolite, glycine betaine, in two strains of SAR11, Candidatus Pelagibacter ubique st. HTCC1062 and Ca. Pelagibacter st. HTCC7211. I found that SAR11 cells had the lowest half-saturation constants (Ks; measure of the environmental concentrations a cell is best at transporting its substrate from) ever measured for a microorganism and its organic substrate. Their Ks values were the same as those measured for raw seawater communities and glycine betaine, demonstrating that SAR11 cells are, indeed, highly efficient at the uptake of substrates from low nutrient concentrations. These experiments made up the first part of my 2019 paper (https://doi.org/10.1111/1462-2920.14649).

For the second question, we hypothesized that the enzymes in SAR11 cells do extra work to compensate for their limited genetic repertoire (i.e., their enzymes are especially multifunctional, performing more functions than they do in other cells). I tested this hypothesis with the glycine betaine transporter in SAR11 cells, finding that it is capable of transporting at least 8 other compounds in addition to glycine betaine. The cells are capable of metabolizing most of these in some manner. I also tested this hypothesis with the metabolism of polyamines (small, ubiquitous nitrogenous compounds) in SAR11 cells. Using mass spectrometry and growth experiments, I found that SAR11 cells can uptake a variety of polyamines via a multifunctional transporter and metabolize them for use as a nitrogen source using multifunctional enzymes. This research was published in a 2021 paper (https://doi.org/10.1128/mBio.01091-21).

We further investigated our second primary question by looking at the lack of transcriptional regulation in SAR11. Generally, bacteria are thought to leave most of their genes turned off until the gene product is needed (e.g., genes encoding the enzymes for degrading lactose are turned off until lactose is present, when they are turned on). However, SAR11, like most oligotrophic marine bacteria (see our review of the subject here: https://doi.org/10.1128/mmbr.00124-22), leave most of their genes turned on all of the time (constitutive expression). We hypothesized that one reason is the lack of motility in most marine oligotrophs, which means that they spend significantly less time in patches of nutrients than bacteria that are motile/chemotactic. Using modeling informed by lab-based experiments, we found that, if SAR11 cells did have transcriptional regulation on the gene for metabolizing L-alanine (a common amino acid), they would only produce 12% of their standing ATP stock upon encountering an L-alanine patch, compared to 880% in cells without transcriptional regulation. Our research on this was published in 2023 (https://doi.org/10.1111/1462-2920.16357).

I've worked on other projects that involve SAR11. One of these is the discovery of a parasitic arsenic cycle in the ocean. This cycle starts when phytoplankton (single-cell photosynthetic microbes) accidentally take up arsenic, a toxic element. Their transporters mistake arsenic for phosphorous due to their similar chemistry. Phytoplankton detoxify arsenic by adding methyl (CH3) groups to the arsenic and exporting it out of the cell. SAR11 cells then take in these methylated arsenic compounds and cut the methyl groups off to gain energy before they export the arsenic out of the cell. We published this research in a 2019 paper (https://doi.org/10.1128/mBio.00246-19).