Evolved phytoplankton on probation

In summer 2013 we tested whether phytoplankton that adapted to environmental stress under laboratory conditions shows a similar fitness increase when exposed to the same stressor in a natural plankton community. The story behind the paper is “long-term”. But I will try to keep it short.

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The paper in Nature Ecology & Evolution is here: http://go.nature.com/2EEQrTE

It all started in 2009. Back then, Kai Lohbeck and I started as PhD students in the BIOACID project at GEOMAR Helmholtz Centre for Ocean Research Kiel. BIOACID aimed to reveal the influence of ocean acidification on marine life and involved many universities and research centres in Germany. One of the key questions by Thorsten Reusch and Ulf Riebesell (both PIs in BIOACID) was if organisms could adapt to ocean acidification through evolutionary adaptation. Kai accepted the challenge to find that out.

The selection experiment to low pH under laboratory conditions run by Kai and Lothar for 2100 generations. Photo: Kai Lohbeck.

Right after starting his PhD, Kai flew to Norway to get fresh isolates of the unicellular phytoplankton species Emiliania huxleyi. “Ehux”, as we call it, is a globally distributed calcifying autotroph with enormous influence on the biogeochemical element cycles in the ocean. Ehux has always been in focus of ocean acidification research due to the pH sensitivity of the calcification process.  Kai used these fresh isolates to set up a long-term laboratory selection experiment where Ehux was supposed to be cultured for hundreds, better thousands of generations under low pH conditions. It took a while before the setup worked but in late 2010 after 500 generations and a year without weekends and holidays, Kai and co-workers could show a partial restoration due to evolutionary adaptation.

In 2013, Kai completed his PhD thesis and a new PhD student, Lothar Schlüter, took over the experimental work. Lothar continued the Ehux experiment until ~2100 generations to reveal the long-term dynamics of Ehux evolution to low pH.

The Sven Lovén Centre (University of Gothenburg) at Gullmarsfjord in winter 2013. Photo: Maike Nicolai, GEOMAR.

In the meantime, BIOACID phase 2 started and I was continuing as a postdoc in the project. One of the central experiments during phase 2 was a long-term ocean acidification experiment where natural plankton communities were enclosed in 10 pelagic mesocosms and five were enriched with CO2 to simulate future ocean carbonate chemistry conditions. The study lasted from winter to summer 2013 on the west coast of Sweden and was hosted by the Sven Lovén Centre of the University of Gothenburg. Revealing the potential of organisms to adapt to low pH within natural assemblages was one of the primary motivations.

The study started a bit bumpy as we had to fight with drifting sea ice, strong currents, and huge salinity variations in Gullmarsfjord. In March we had finally regained control and were able start our experiment which lasted for 113 days until the end of June.

Not such a comfortable place for mesocosms. Gullmarsfjord in February 2013 filmed by Michael Sswat.

In May, halfway through the experiment, we had a memorable (for me at least!) science meeting. We were talking about Ehux blooms that typically occur in the North Atlantic right at that time of the year and whether or not we would also observe them in Gullmarsfjord. I had to think of the long-term experiment with Ehux cultures and I was wondering if we could connect this with our long-term experiment in Gullmarsfjord. It would be a great chance to test if the adaptation to low pH Kai, Lothar, and co-workers found under lab conditions would bring a competitive advantage for the cells when exposed to low pH in a natural plankton community. And the circumstances were ideal to approach this question. We had the long-term lab cultures at GEOMAR and natural plankton communities that had seen low pH conditions for almost 3 months already. The timing seemed to be perfect as well since we had Ehux bloom season. Furthermore, Ehux can be easily distinguished from bulk phytoplankton in the flow cytometer due to particular optical properties. So we had all the ingredients to address this exciting question and thought let’s go for it!

A couple of days (and an estimated 1 million discussions) later Lothar subsampled 10 cell cultures (5 control and 5 low pH lineages) from the lab experiment and sent them to the Sven Lovén Centre. Meanwhile, I collected seawater from one ambient and one low pH mesocosm and distributed it in 30 “microcosm” bottles each. The Ehux cultures were then incubated for 26 days in these microcosms with the plankton communities in a full factorial design. To our astonishment all 10 Ehux lineages were doing relatively well in the natural plankton communities, despite the 4 years of culturing in the lab. However, the low pH adapted lineages were not performing better than the control lineages in the low pH plankton communities. Thus, adaptation to low pH under laboratory conditions did not improve the “fitness” in a natural plankton community. This was a key finding as it emphasizes that adaptation to stress under simplified lab conditions does not necessarily lead to equivalent fitness gains in an ecological context.

Microcosms preparation and installation for 26 days on a plankton wheel. Photos: Jana Meyer, GEOMAR.

However, at least equally interesting was our second major finding: Some of the lineages were able to dominate the plankton communities while others almost went extinct during the 26 days experiment. The large difference in the lineages’ ability to survive in the natural plankton communities came as a surprise since all 10 lineages originated from the same genotype only 1700 generations ago. It demonstrated that highly variable competitive abilities can evolve extremely fast, faster than ongoing climate change.

Lennart Bach

Researcher, GEOMAR Helmholtz Centre for Ocean Research Kiel

Marine biologist from Kiel interested in plankton ecology and marine biogeochemistry