How do eukaryotic CO2 fixers co-exist with faster growing prokaryotic CO2 fixers in the oligotrophic ocean covering 40% of Earth?

Lead Research Organisation: National Oceanography Centre
Department Name: Science and Technology

Abstract

The principal aim of the proposal is to explain the ecological basis of the most extensive biome on Earth - co-existence of eukaryotic CO2 fixers with faster growing prokaryotic CO2 fixers in the open oligotrophic ocean. Eukaryotes dominate CO2 fixation in most of Earth's biomes, e.g. terrestrial, freshwater and some marine (coastal and polar waters), with one but major exception: the oligotrophic oceanic gyres, covering 40% of Earth. Why have energetically superior eukaryotes been unable to outgrow prokaryotes despite millions of years of co-evolution in the gyres?
We hypothesise that co-existence of CO2 fixing eukaryotes and prokaryotes is sustained by episodic nutrient pulses into the surface sunlit waters complemented by feeding of CO2-fixing eukaryotes on prokaryotes, i.e. bacterivory. Using the combined expertise of our research team strengthened by novel experimental approaches we will address the following questions: What is the impact of nutrient pulses on growth rates of CO2-fixing prokaryotes and eukaryotes? How do nutrient pulses affect bacterivory? Is selective feeding by CO2-fixing eukaryotes a mechanism for controlling growth of CO2-fixing prokaryotes?
We will find out how general the answers to the above questions are by focusing on experimental work in the subtropical gyres of the Atlantic and Pacific Oceans, which comprise nearly three quarters of the total oligotrophic open ocean area. The three gyres we will investigate are of different geological ages and differ in composition of depleted inorganic nutrients. We will use isotopic tracers in combination with flow cytometric sorting to directly measure impact of nutrient pulses on microbial group-specific growth rates and bacterivory rates. Morphology, taxonomic identity and physiological potential of flow sorted microbial groups will be characterised by ultra-structural, molecular and metagenomic analyses. The effects of nutrient pulses on cellular biomass of CO2 fixing prokaryotes and eukaryotes will be assessed by electron microscopy of flow sorted cells coupled with energy dispersive X-ray spectroscopy.
The experimental evidence will be synthesised into a generic concept to explain the mechanism of co-existence of the smallest eukaryotic and prokaryotic CO2 fixers of increasing global biogeochemical significance owing to expansion of the oligotrophic ocean under the influence of modern climate changes. Thus, the project will test the extent of inorganic nutrient control of biological CO2 fixation in the largest Earth's biome.

Planned Impact

The proposed project will answer several basic biogeochemical and ecological questions: Why are oligotrophic gyres in fine balance between net auto- and heterotrophy? How can nutrient availability affect co-existence of key prokaryotic and eukaryotic CO2 fixers in the oligotrophic ocean, which is expanding with current climate change? And how could the competitive exclusion law be breached in the oligotrophic ocean? By providing experimental evidence to substantiate those answers the project will test the extent of inorganic nutrient control of biological CO2 fixation in the largest Earth's biome. The results of those tests will evaluate how universal is the paradigm that marine biological CO2 fixation is ultimately controlled by availability of inorganic nutrients. This paradigm is pivotal for most biogeochemical models of marine systems, including the ones developed by the Met Office and used to forecast changes in ocean biogeochemical cycles. In addition to environmental scientists the basic outcome of the project could be of interest to a much broader community of marine specialists at institutions, consultancies and government departments as well as to the general public and their representatives in parliament who are concerned about our marine environment and its integrity.

Owing to its remoteness the oligotrophic ocean is a part of Earth's surface least affected by human activities. This ocean is populated by microbes adapted to optimally extract very low levels of nutrients. The proposed study will provide experimental and metagenomic evidence about how those microbes concentrate and transport these nutrients. Once their mechanism of high-affinity transport is elucidated it could be used in biotechnology both for efficient sequestration of rare ions (e.g. rare earth metals) from ultra-dilute solutions as well as for targeted water purification.

To disseminate our research to the beneficiaries and general public Manuela Hartmann (MH) will attend the "Engaging the public with your research" training course at NERC and will be encouraged to participate in the Royal Society MP pairing scheme (https://royalsociety.org/training/pairing-scheme/). In addition, we will contribute to the NERC publication Planet Earth, widely read by a broad range of scientists, commercial organisations, MPs and civil servants as well as present our work at the Royal Society summer science exhibition, NOCS open days and Marine Life talks. The NOCS Communications department will be used to interact effectively with media and public. MH also plans to present science to the public at Café Scientifique (http://cafescientifique.org), a scheme developed by the British Council.

The Natural History Museum (NHM) hosts over five million visitors a year, and offers a wide range of ways in which they can develop their biological understanding and take part in directed activities. We will use NHM-hosted public engagement activities and expertise to present our results in diverse and relevant ways to different audiences, including school and university students, amateur biologists, and the generally interested public. It is also currently re-developing its website (opening in 2015) which will include more methods of communication. Ongoing activities include NatureLive (http://www.nhm.ac.uk/visit-us/whats-on/daytime-events/talks-and-tours/nature-live/index.html), Science Uncovered (http://www.nhm.ac.uk/visit-us/whats-on/after-hours/science-uncovered/index.html), the newly devised Universities Week (http://www.nhm.ac.uk/about-us/news/2014/june/universities-week-gets-off-to-an-explosive-start131363.html), and the popular NHM Twitter account. In addition, we will work with the Angela Marmont Centre (http://www.nhm.ac.uk/visit-us/darwin-centre-visitors/marmont-centre/) and NHM press office. The high quality electron microscopy images generated as part of the research will be displayed at suitable sites around the NHM.

Publications

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NE/M014363/1 01/10/2015 31/12/2017 £390,824
NE/M014363/2 Transfer NE/M014363/1 01/04/2018 31/03/2022 £336,022
 
Description The ubiquitous SAR11 and Prochlorococcus bacteria manage to maintain a sufficient supply of phosphate in phosphate-poor surface waters of the North Atlantic subtropical gyre. Furthermore, it seems that their phosphate uptake may counter-intuitively be lower in more productive tropical waters, as if their cellular demand for phosphate decreases there. By flow sorting 33P-phosphate-pulsed 32P-phosphate-chased cells, we demonstrate that both Prochlorococcus and SAR11 cells exploit an extracellular buffer of labile phosphate up to 5-40 times larger than the amount of phosphate required to replicate their chromosomes. Mathematical modelling is shown to support this conclusion. The fuller the buffer the slower the cellular uptake of phosphate, to the point that in phosphate-replete tropical waters, cells can saturate their buffer and their phosphate uptake becomes marginal. Hence, buffer stocking is a generic, growth-securing adaptation for SAR11 and Prochlorococcus bacteria, which lack internal reserves to reduce their dependency on bioavailable ambient phosphate.
Exploitation Route Through publications and data archived at BODC
Sectors Education,Environment