Nutrient cycling propels the oceans' engine

Marine microbial phototroph heterotroph interactions are sustained by nutrient cycling

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Oceans, the largest biomes on Earth are major drivers of global biogeochemical cycles. Contained within are a myriad of marine unicellular photosynthetic microbes (such as the marine cyanobacteria Prochlorococcus and Synechococcus), which are responsible for half of the planet's primary production and half of the oxygen we breathe. Most of the energy that is introduced into the oceans by these photosynthetic algae is in the form of organic matter that then sustains the rest of the food web, from micro- to macro-organisms. The interactions that occur between phototrophic microorganisms and heterotrophic bacteria, the latter organisms being those that use organic carbon, are vital for maintaining the oceans’ nutrient balance via the so-called microbial loop that ultimately feeds higher organisms.

When I first started working with Synechococcus, almost six yeast ago, I soon become aware of the difficulty of growing these relevant marine phototrophic organisms. They grew so slowly and were so picky with the light, media, etc! Having worked in the past with heterotrophic marine bacteria, it was hard for me to understand the fact that most marine photosynthetic cultures are ‘not axenic’ or, in other words, also contain heterotrophic bacteria in the cultures. Nevertheless, those cultures that contain heterotrophic bacteria grow better and for a much longer time than those that are ‘axenic’ (in pure culture). For example, it is amazing that we currently have an eight year old culture (our lab ‘pet’) that is growing as happily as the first day. Why?  

Figure: Eight-year old Synechococcus culture (the lab ‘pet’) and fluorescent microscopy images showing Synechococcus cells (bright orange due to the auto-fluorescence produced by their photosynthetic pigments) in axenic culture, and non-axenic culture i.e. with heterotrophic bacteria (stained blue by DAPI).

The answer was relatively simple but had never before been demonstrated with experimental data. Marine cyanobacteria are incredibly adapted to marine conditions and, as Dave Scanlan says, they are really good at being ‘photosynthesising and carbon fixing machines’. However, they are generally not very good at carrying out other functions. Photosynthetic organism cultures ‘leak’ and, in this case, axenic cultures become rapidly intoxicated by their own ‘waste’ and die. However, in co-culture with heterotrophic bacteria these heterotrophs detoxify the media, sustaining Synechococcus cultures for long periods (up to years as shown by the lab pet).

But… how is this relevant to the real world? A build-up of such levels of organic matter in the oceans is highly unlikely. All interaction studies to date have been carried out in nutrient-rich media where the phototrophic organism thrives and reaches high cell densities. But what happens in natural seawater where nutrients are scarce? To be honest, I didn’t think my model system would survive in seawater! When I set it up, it was like looking at seawater, translucent with nothing in it. But flow cytometry measurements were telling me bacteria were there and, what was more interesting, the heterotrophs and phototrophs were reaching a ‘stable state’ with abundance ratios similar to those observed in the oceans. We showed via high throughput proteomics and nutrient analyses that in these nutrient poor systems both organisms are mutually benefiting from each other as the heterotroph specialises in the use of organic matter releasing inorganic nutrients that are then rapidly taken up by the phototroph to continue photosynthesising and fixing carbon. The novelty of this study resides in dissecting the nutrient exchange occurring in long-term microbial interactions under natural oligotrophic conditions and the collaborative interaction that takes place between these niche partitioned groups of microorganisms.

Nevertheless, there are still many unknowns and a lot of work ahead!

Our Nature Microbiology paper is here:

Joseph Alexander Christie-Oleza

Assistant Professor, University of Warwick