How algae hack it in the ocean

Approximately half of global photosynthesis happens in the ocean. Open ocean regions are often referred to as “deserts” – and yet this is where the bulk of marine photosynthesis happens. The tiny algae that thrive in these regions have specialized ways of rapidly adjusting to environmental variations that integrate evolutionary conserved and phylogenetically more recent proteome systems to sustain growth and carbon dioxide uptake.

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The paper in Nature Microbiology is here: 

Open ocean regions are often referred to as “the deserts of the oceans”…of course this isn’t really a fair characterization because what we know now is that there is fast turnover in these ecosystems. There is a continual use and reuse of nutrients so that they are tied up in active growth of cells and not just sitting around as free molecules in the water. Needless to say it is true that what remains as free molecules in the water is very very little. Phosphate and nitrogen, those two oh-so-common fertilizers used in agriculture, are typically below chemical assay detection limits in these ecosystems. Predictions of the future suggest nutrient availability may be even lower in many of these regions as the oceans warm, due to increased stratification.

Our goal was to understand how eukaryotic algae deal with this competitive environment. We set our bar at: working with an environmentally-relevant emerging model system, working at phosphate concentrations one might measure in the open-ocean, and looking at biological processes of living, actively GROWING cells – whose growth was limited by phosphate – a nutrient we know is depauperate in much of the North Atlantic after springtime. What can be done more readily in the lab is to observe the transition to starvation – but let’s face it – if you are not growing out there you are toast! Someone will come along and gobble you up – end of the line, bloom demise or some other awful fate. Our bar required that we implement a high-tech system for providing a continuous supply of medium (in and out-flow, sterile) and then why not also have fully adjustable temperature, CO2, light and frequent measurements of photosynthetic activity? So that is the photo-bioreactor system we worked with, alongside performing proteomic, RNA-seq and biophysical analyses.

Co-author Lisa Sudek working with the photo-bioreactors

Our study went off without a hitch (depending on how you define that) – and the results reveal an elegant remodeling that provisions growth rates just the same as measured in the North Atlantic after springtime – and phosphate drawdown to the same levels. From the oceanographers perspective our results highlighted the quite inconvenient truth that, even for the proteins that changed significantly under the transitions we tested, many gene transcripts for these proteins did NOT change significantly! This is no surprise for the eukaryotic cell biologist in the room…but it certainly calls for caution in terms of inferences we draw from metatranscriptomes. On the bright side, we found that a fascinating set of evolutionary conserved and phylogenetically recent proteome systems formed the protein network that sustains the alga’s growth during low-phosphate times, and allow it to respond quickly to a fresh pulse of phosphate, rapidly increasing replication even in the early stages of resupply. 

An ancient light-harvesting-associated protein stole the show by throwing away damaging excess light energy as heat throughout extended phosphate limitation, allowing the major light harvesting components to stay up and running, so that the moment a pulse of phosphate came along the alga, Micromonas, could grab it and grow. This protein has well established roles in mitigating high light stress – a light level we didn’t go near. At first we wondered if differences in our results from prior marine algal studies were something do with the green alga we work on being evolutionarily close to land plants, while most prior studies were on very distant unrelated phytoplankton. But really, for something like photosynthesis, which shows such powerful biological conservation in its machinery, this seemed unlikely. 

First author Jian Guo hard at work

So then we thought it must be because LIMITED nutrient supplies are not the same as NO nutrients. After all, much of the human population lives in a malnourished state and does amazing things every day, but a starved population is on a tragically different trajectory. But, on further mulling, we landed on the idea that perhaps we have the concept of “stressed” cells in the environment all backwards. What if we took the audience reading this blog and made them the treatment (“limited” population) and our comparator control was a population that eats only at McDonald’s (“replete” population) akin to what happens in most culture media (Supersize Me). From there, every molecular response of that Blog-reading-crowd is termed a “stress response” and the Supersize is termed “normal response”, representative of a normal physiology. OK, I guess a few folks reading this blog might feel stressed, but our basic biological physiology is probably more on the normal spectrum for a healthy human population than the Supersize. Bottom line, our study has captured a picture of how these tiny widespread algae acclimate and adjust to the dynamics and often nutrient-limited conditions of the open ocean…and that provides a platform (or a starting point!) for really interpreting field biology and modeling responses in future oceans.

Did I mention that along with the many other kinds of life events that might occur, the first author had her second baby during the study, the last author had her first and second kids and there was a sprinkling of other new parents on the team? Oh, and do let us forget that the robot jammed at the sequencing center and destroyed most of the hard-earned  RNA samples, for an experiment that required mostly daily attention, love and care over more than 50 days… with a few other experimental drama points on top…and years to go in the analysis. Grit, grit was an important ingredient.

First author Jian Guo in play mode with her children

Thanks and Credits to: Lorrie Klosterman (Micromonas water colour), Charles Bachy for creating McMicromonas with Lorrie’s water colour, Todd Walsh (co-author Lisa Sudek working with the photo-bioreactors), and Charles Bachy for comments on this blog. Also shown, photos of first author Jian Guo hard at work and hard at play! …and many thanks to the amazing team of collaborators involved in the project!  

Alexandra Worden

Professor, Monterey Bay Aquarium Research Institute