How do eukaryotic CO2 fixers co-exist with faster growing prokaryotic CO2 fixers in the oligotrophic ocean covering 40% of Earth?
Lead Research Organisation:
Scottish Association For Marine Science
Department Name: Dunstaffnage Marine Laboratory
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.
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.
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
Schoffelen NJ
(2018)
Single-cell imaging of phosphorus uptake shows that key harmful algae rely on different phosphorus sources for growth.
in Scientific reports
Kamennaya NA
(2018)
"Pomacytosis"-Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae.
in PLoS biology
Leles S
(2019)
Sampling bias misrepresents the biogeographical significance of constitutive mixotrophs across global oceans
in Global Ecology and Biogeography
Dabrowska A
(2019)
Impact of ferromanganese ore pollution on phytoplankton CO2 fixation in the surface ocean.
in Marine pollution bulletin
Thomsen HA
(2020)
Loricate choanoflagellates (Acanthoecida) from warm water seas. VII. Calotheca Thomsen and Moestrup, Stephanacantha Thomsen and Syndetophyllum Thomsen and Moestrup.
in European journal of protistology
Lange P
(2020)
Radiometric approach for the detection of picophytoplankton assemblages across oceanic fronts
in Optics Express
Giljan G
(2020)
Bacterioplankton reveal years-long retention of Atlantic deep-ocean water by the Tropic Seamount.
in Scientific reports
Kamennaya NA
(2020)
Accumulation of ambient phosphate into the periplasm of marine bacteria is proton motive force dependent.
in Nature communications
Thomsen H
(2020)
Loricate choanoflagellates (Acanthoecida) from warm water seas. VI. Pleurasiga Schiller and Parvicorbicula Deflandre
in European Journal of Protistology
Kamennaya NA
(2022)
Flow cytometric sorting of loricate choanoflagellates from the oligotrophic ocean.
in European journal of protistology
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| Project Reference | Relationship | Related To | Start | End | Award Value |
|---|---|---|---|---|---|
| NE/M014363/1 | 30/09/2015 | 31/12/2017 | £390,824 | ||
| NE/M014363/2 | Transfer | NE/M014363/1 | 31/03/2018 | 31/12/2023 | £336,022 |
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| Exploitation Route | n/a |
| Sectors | Education Environment |
| Description | This is a duplicated grant entry. Please see the first entry for details. Further details added Apri 2024: The strength of the biological carbon pump appears not to be linked to phytoplankton size as had been previously hypothesized. This is of potential relevance to the parameterisation Earth systems models in projecting the draw-down of atmospheric CO2 (see: Serret, P., J. Lozano, C. B. Harris, P. K. Lange, G. A. Tarran, G. H. Tilstone, E. M. S. Woodward and M. V. Zubkov (2023). "Respiration, phytoplankton size and the metabolic balance in the Atlantic gyres." Frontiers in Marine Science 10). Results provide a benchmark for testing the predictions of size-based plankton models and for assessing future, climate-related shifts in phytoplankton size structure in both coastal and oceanic regions of the Atlantic Ocean (see: Phongphattarawat, S., H. A. Bouman, M. W. Lomas, S. Sathyendranath, G. A. Tarran, O. Ulloa and M. V. Zubkov (2023). "Ecophysiological basis of spatiotemporal patterns in picophytoplankton pigments in the global ocean." Frontiers in Marine Science 10.). Work shows that bacteria accumulate phosphate (an essential component of all living cells for their DNA and energy production) to high concentrations in their periplasm. This is a seminal finding that has wide academic interest. One fundamental implication of this 'chemical' accumulation of phosphate is that it may be a fundamental component of how life emerged from the prebiotic soup, as phosphate will accumulate at surfaces where there is a balancing flow of protons in the other direction. Critically, it does not require any biological mechanisms to accumulate the phosphate (see: Kamennaya, N. A., K. Geraki, D. J. Scanlan and M. V. Zubkov (2020). "Accumulation of ambient phosphate into the periplasm of marine bacteria is proton motive force dependent." Nature Communications 11(1): 2642.). Knowledge of protistan biodiversity and development of a collection of novel protists during this CO2 fixers has been leveraged as a core hypothesis to effect biocontrol of seaweed disease and pathogens in the UKRI-BBSRC grant FABRICS (see further funding section). |
| First Year Of Impact | 2020 |
| Sector | Education,Environment,Other |
| Description | FABRICS: Facilitating Algal Biotechnology with Rhodophyta for Intensive Culture Systems |
| Amount | £387,806 (GBP) |
| Funding ID | BB/Z515309/1 |
| Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
| Sector | Public |
| Country | United Kingdom |
| Start | 07/2024 |
| End | 08/2026 |
| Title | Direct PCR from flow sorted cells |
| Description | Performing polymerase chain reactions (PCR) of a small number of cells is challenging, with established protocols often exhibiting low and taxonomy-biassed success rates in real-world scenarios. Here we developed an optimised protocol for direct PCR from flow-sorted cells, significantly enhancing success rates. Our method involves dedicated micro-liter scale lysis steps, which combine chemical (alkaline lysis buffer) and physical (freeze-thaw) cell disruption techniques, followed by PCR with high-fidelity polymerases. |
| Type Of Material | Technology assay or reagent |
| Year Produced | 2022 |
| Provided To Others? | No |
| Impact | Our method to molecularly characterize flow-sorted cell populations has been successfully applied to complex laboratory systems, and environmental samples, including those from the Mediterranean and Red Sea (2022). We have validated the effectiveness of our method across the eukaryotic tree of life, showing its capability to handle challenging cell types, such as those with thick cell walls and small genomes. Our method is widely applicable and enables molecular fingerprinting of cell populations using only a few sorted cells. This capability opens avenues for studying trophic interactions, both in controlled laboratory settings and natural field environments. This method will be disseminated upon publication. |
| Title | Ecology-driven isolation and culturing techniques of hard-to-culture mixotrophs |
| Description | Natural marine water samples are collected by Niskin bottle or other; samples are dispensed to multi-well plates and inoculated with a range of environmentally relevant and locally isolated prey organisms, such as ultra-small bacteria (Vibrio sp. COLL2) to stimulate the growth of bacterivorous mixotrophs, or with picoeukaryotes (Micromonas, Nephroselmis, and others) to stimulate growth of eukaryvorous mixotrophs. Once the preferred prey is determined, enrichment cultures are repeatedly refreshed with the prey to achieve clonal cultures of mixotrophs or predatory heterotrophs. |
| Type Of Material | Biological samples |
| Year Produced | 2023 |
| Provided To Others? | No |
| Impact | The majority of phagotrophic protists are notoriously difficult to culture, often labelled as 'unculturable', resulting in limited data on their general biology. This represents significant gaps in our understanding of eukaryotic biodiversity, ecology, and evolution. We developed effective isolation and culturing techniques that led to the establishment of a diverse culture collection encompassing various enigmatic phagotrophic and phago-mixotrophic protists (ranging in size from 1.3um to 10 um). Our collection from coastal and open-ocean systems, includes members from all major eukaryotic lineages, including among the first stable cultures for Provora, Marine Alveolate lineage (MALV), and Marine Stramenopile (MAST). These lineages hold significant environmental importance, yet prior to our work, stable cultures were largely unavailable. Our innovative culturing techniques have enabled empirical laboratory studies, allowing for the documentation of morphology, behavior, and prey preference, revealing novel ecological roles of several novel and other enigmatic phagotrophs. By leveraging our ecology-informed culturing techniques, we've been able to scale up key strains in our collection that unlocked the application of biomass-demanding techniques, such as genome sequencing using PacBio and transcriptomic interrogation through RNA-seq. The ecological principles underlying our culturing techniques are thought to be universal, suggesting their applicability to other environments, such as human or life-stock gut microbiomes, agricultural systems, where uncultured protists play important roles. Our culturing techniques not only overcome major challenges but also pave the way for further research into the biology, genetic makeup, and ecological significance of enigmatic protists. Our techniques will be disseminated in detail through publication |
| Title | Semi-supervised binning of long-read DNA data for improved assembly of multiple genomes |
| Description | The current efforts to generate high-quality draft genomes of novel mixotrophs or predatory protists face significant challenges due to the complex nature of their cultures. These cultures often consist of multiple organisms, including bacteria or other eukaryotes serving as prey, each present in varying abundances and possessing genomes of different sizes and complexities. Using existing genome assemblers, it is very difficult to accurately assemble and distinguish multiple eukaryotes from these 'metagenomic'-like datasets, particularly in the absence of reference genomes. Additional challenges arise when dealing with complex communities comprising multiple eukaryotes with diverse or poorly characterised genetic background, each having their own organelles (plastid and or mitochondria) or other genetic elements that have never been seen before. Therefore, we have developed a semi-supervised bioinformatic binning approach designed to classify each sequencing read in long-read genomic sequence datasets, before genome assembly. Our tool leverages the discriminative power of kmer-frequency based compositional data to identify the origin of each read, distinguishing genetic elements such as nulcear genomes, organelles and bacteria. To achieve this, we employ a non-linear dimensionality reduction technique, Uniform Manifold Approximation and Projection (UMAP), which projects the high dimensional kmer data into a 2D space, enabling both in unsupervised (dbscan, hdbscan) or supervised (lasso-selection tool and web interface) binning of the read clusters. Given the large size of long-read datasets, often containing hundreds of milions of reads, our tool is implemented in a memory-efficient manner and has demonstrated scalability to real-world and state-of-the-art genomic datasets. Once the reads are binned, they are separated into distinct fastq files and can be used as input for the assembler of choice. We have shown that binning genomic data on the read level prior to assembly substantially improves the recovery of genomes compared to more traditional metagenomic assembly workflows. |
| Type Of Material | Technology assay or reagent |
| Year Produced | 2023 |
| Provided To Others? | No |
| Impact | Facilitating more accurate reconstruction of genomes from complex datasets , we anticipate that our tool is applicable to a wide range of studies across different fields and research settings. Our tool enables researchers to uncover novel genetic elements, organelles, and microbial interactions that may have been previously overlooked. This could lead to the discovery of new biological functions, metabolic pathways, and ecological relationships. The tool's user-friendly web interface, including features such as a lasso-selection tool for supervised binning, makes it accessible to researchers with varying levels of bioinformatics expertise, promoting broader adoption and utilization. Its modular implementation in Python, using current libraries such as NumPy, sci-kit-learn, allows for easy maintenance, further development, and distribution across different computing facilities. The tool has been essential in disentangling genomic datasets as generated by this grant, and will be presented in a future publication and open-source code will be made available on GitHub. |
| Title | Pacbio Hifi genomic & transcripomic data of Katablepharids and their mixotrophic prey |
| Description | Cryptomonads, a group of single-celled eukaryotes comprised of both photosynthetic and non-photosynthetic species, often retain the ability to predate on bacterial cells through phagocytosis and hence are a major lineage of mixotrophs. Moreover, cryptomonads harbor a red algal-derived plastid of secondary origin and were recently proposed to be the ancient donor of red-algal-derived plastids in the other 'chromalveolate' lineages through a series of further endosymbiosis events, unified under the "Rhodoplex" hypothesis. However, no extant cryptophyte, nor its plastid-lacking sister lineage Goniomonadea were ever shown to prey on eukaryotes, yet this ability is a prerequisite of secondary endosymbiosis. Another closely related group, of heterotrophic as well as kleptoplastidic (stealing plastids) eukaryvorous protists, the Katablepharids, hold great promise to help resolve the evolutionary pathways, and events that have occurred at the outset of the secondary endosymbiosis event that gave rise to photosynthetic cryptomonads. Given the relevance of Katablepharid genomes in the elucidation of early secondary plastid acquisition in cryptophytes, we generated PacBio Hifi DNA and Illumina RNA-seq datasets for two Katablepharis isolates to generate the first high-quality draft genome assemblies of the Katablepharid lineage. We also sequenced the genome and transcriptome of its prey, a green algal isolate from the mixotrophic Nephroselmis genus, and notably the origins of the kleptoplast in other Katablepharid groups. Mixotrophy for our Nephroselmis isolate was confirmed in our laboratory experiments, and our genome-sequenced strain will be further utilized in follow-up transcriptomic experiments aimed at elucidating transcriptional regulation underlying mixotrophy, and the establishment of a green-algal mixotrophy model system. |
| Type Of Material | Data analysis technique |
| Year Produced | 2023 |
| Provided To Others? | No |
| Impact | These genomic and transcriptomic datasets, together with our stable cultures facilitate the development of laboratory model systems for research in 1) the origins of secondary plastids in cryptophytes, 2) the evolutionary positioning of kablepharid lineage, 3) their mechanisms for eating eukaryotic prey, and 4) the mechanisms underlying mixotrophy in the green-algal lineage (Nephroselmis). |
| Title | Pacbio Hifi genomic & transcripomic data of minute and early-divergent Stramenopiles |
| Description | Stramenopiles (heterokonts), represent a major group of eukaryotes, encompassing various photosynthetic (e.g., kelp, diatoms), mixotrophic (ochrophytes), and parasitic (oomycetes) organisms. While photosynthetic Stramenopiles, thought to comprise a single monophyletic group Ochrophyta, dominate the described species, early-divergent lineages of Stramenopiles include numerous poorly understood hetreotrophic nanno-flagellates, contributing significantly to bacterivory in the environment. Nested bewteen ochrophytes and oomycetes, the Bigyromonadea group contains the lesser-known Developea and parasitoid Pirsonieales, exhibiting transitional lifestyles between bacterivory, eukaryvory, and parasitism. Free-living Bigyromonadea may harbor ancestral characteristics shared with parasitic oomycetes or the ancestors of ochrophytes. Recognising the importance of Developea genomes in elucidating early secondary plastid acquisition in Stramenopiles and the evolution of parasitism in oomycetes, we generated PacBio Hifi DNA and Illumina RNA-seq datasets for a free-living Developayella isolate to generate the first high-quality draft genome assemblies for this group. Additionally, using the same sequencing technologies, we sequenced the genome of a basal Stramenopile, representing the first isolate of a novel genus of bacterivorous nanno-flagellates, similar to MAST-lineages. Characterised by its minute cell size (1.3 microns), exclusively bacterivorous lifestage, and morphology resembling heterokont zoospores (including that of kelp) as well as one of the most abundant predators in the oceans, this organism presents attractive features for comparative analyses regarding lifestyle differentiation in Stramenopiles, such as the acquisition of eukaryvory, and acquisition of secondary plastids in Ochrophytes. Our genome-sequenced strains will be further utilized in follow-up transcriptomic experiments aimed at elucidating transcriptional regulation underlying bacterivory and eukaryvory. Moreover, they will facilitate the development of laboratory model systems for studying the trophic interactions and evolutionary dynamics within stramenopiles. |
| Type Of Material | Data analysis technique |
| Year Produced | 2023 |
| Provided To Others? | No |
| Impact | These genomic and transcriptomic datasets, together with our stable cultures facilitate the development of laboratory model systems for research in 1) the origins of secondary plastids in Ochrophytes, 2) mechanisms that allow prey capture and digestion of bacterial and/or eukaryotic prey, and 3) linking genetics with key phenotypic traits associated with lifestyle transitions in Stramenopiles (autotroph, heterotroph, mixotroph, and parasite). Moreover, having sequenced for the first time a set of understudied lineages, our dataset allows to further resolve the phylogenomic relationships within Stramenopiles. |