New Study Explores Unique Ways Diatoms Metabolize Nitrogen, Enabling Them to Thrive in Dynamic Environments
(La Jolla, California)—October 7, 2019—A team led by scientists from the J. Craig Venter Institute (JCVI), Scripps Institution of Oceanography, and the Systems Biology Research Group in the Department of Bioengineering at the University of California San Diego has discovered that diatoms, a diverse type of photosynthetic microalgae, are unique in almost every aspect of nitrogen metabolism when compared to other eukaryotic organisms. Since diatoms are crucial for the health of global ocean waters and also produce around 20% of global oxygen, a better understanding of these important phytoplankton is key for healthy ocean ecosystems.
For the study, published in Nature Communications, the team compared the nitrate sensing, regulatory machinery, and overall configuration of nitrogen assimilation and metabolism of the model diatom Phaeodactylum tricornutum to that of other eukaryotes, including yeast, other fungi, green algae, plants, and multicellular animals. They used a diverse combination of experimental and computational approaches, including comparative and functional genomics, phylogenetic analyses, physiology and stable isotope metabolic flux labeling, proteomics, and genome-scale flux balance modeling.
The team notes that when environmental conditions related to nutrient and light availability (often coinciding with upwelling events) are ideal, diatoms take in more nitrate, the dominant nitrogen source during active upwelling, than they need for growth, thereby denying this key nutrient to others living in this environment. The researchers measured the transcriptional response of diatoms to different nitrogen sources on minute and daily time scales to capture the specific response of different genes and proteins to nitrate compared to other nitrogen sources. They found that some genes are highly sensitive to nitrate, while others are responsive to elevated or depleted levels of nitrogen. They also identified specific DNA elements in the upstream regions of these genes that control their responsiveness to differing nitrogen sources and levels. Sometimes genes appeared to be dually regulated by DNA elements responsive to signals for nitrate and for nitrogen depletion.
The team also conducted detailed analyses on the evolutionary origins of dozens of individual components of diatom nitrogen metabolism. Diatoms arose from an evolutionary process known as secondary endosymbiosis, while plants and other phytoplankton in the green lineage arose from a primary endosymbiosis. This means diatoms inherited their chloroplast from eukaryotic algae and not photosynthetic bacteria. As a result, diatoms retain unique combinations of traits that are animal-like, plant-like, and bacteria-like, hallmarks of which can be seen in the phylogenies of modern-day diatom genomes.
In this study, the team identified which key enzymes were derived from which endosymbiotic partner and noted some of the biological capabilities of the partners prior to endosymbiosis. These analyses help to provide context for evolutionary developments that occurred after diatom chloroplast acquisition, such as duplications of genes that appear to enable delivery and transport of nitrogen and carbon from the mitochondria to the chloroplast.
Lead author Sarah R. Smith, Ph.D., Staff Scientist at JCVI stated, "We've known for some time that diatoms do things differently from other classes of algae when it comes to taking in and metabolizing nitrogen. We generally suspected that their differences had something to do with their unique evolutionary history. What we didn't know was where these traits originated from, nor how they were combined functionally to give diatoms an advantage over other groups. Now we do."
The big advantage diatoms have lies in the details of their metabolism. Once nitrogen is inside the cell, a complex dance of energy and carbon supply occurs to ensure that the cellular components that fuel growth, manage light absorption, and regulate stress responses are manufactured appropriately. This dance is choreographed differently in diatoms than it is in green algae (ancestors of land plants). Simply put, diatoms have more extensive metabolic links between major energetic organelles (chloroplasts and mitochondria) than was appreciated previously. This configuration allows diatoms to couple nitrogen status to growth, allowing for both efficient utilization of new nitrogen and recycling/reuse of the nitrogen already in their cells if very low or scarce nitrogen is encountered.
Previous work from Andrew E. Allen, Ph.D., senior author and a joint professor at JCVI and Scripps Oceanography, highlighted the unusual evolutionary origins of the diatom urea cycle and revealed surprising commonalities between diatoms and animals compared to plants and green algae. That work resulted in the discovery of the diatom urea cycle as an apparent repackaging and redistribution hub for nitrogen metabolites, in contrast to animals where it functions to excrete excess nitrogen waste. This study goes much further to show how the diatom urea cycle, which functions in the mitochondria, is integrated with and connected to nitrate assimilation in the chloroplast as an arginine biosynthesis pathway unlike that of any other known eukaryote.
Allen commented, "In this study we traced metabolites and energy fluxes through particular enzymes and subcellular compartments. This detailed knowledge of cellular function is absolutely indispensable for understanding the ocean nitrogen cycle, and for bioengineering and bio design strategies aimed at harnessing the potential of diatoms for industrial production of high value products related to food, fuel, and biomaterials."
Bernhard O. Palsson, a coauthor from the Systems Biology Research Group in the Department of Bioengineering at UC San Diego remarked, "Studies such as this one, targeted to enigmatic but promising organisms such as diatoms, which combine genome-enabled systems biology and functional genomics, present a tremendous opportunity and blueprint to develop sustainable and economical feed and fuel production from algae within 10 years."
How and why diatoms evolved these particular abilities, while other phytoplankton did not, is an open question and one of continued study for the team. It is likely that the evolutionary history and subsequent adaptations of diatoms as compared to other algae might give some answers.
Diatoms rose to prominence because of adaptations that allow them to take advantage of unique opportunities and challenges in the ocean environment. As the climate changes, due in large part to burning fossil fuels, some ocean regions will become warmer, more acidic, and more stratified, whereas other regions could experience more frequent and more intense upwelling. The ecological forecast for diatoms, along with the production of the life-sustaining oxygen they produce, is uncertain. The team is continuing to study diatom biology not only with the hopes of increasing understanding and survival of these key phytoplankton, but to better harness their unique metabolism to arrive at sustainable solutions to key global problems like production of high-quality proteins and renewable biofuels.
The research team also included Miroslav Obornik, Institute of Parasitology and University of South Bohemia, Czech Republic; Alisdair Fernie, Max Planck Institute of Molecular Plant Physiology; and Zoran Nikoloski, Institute of Biochemistry and Biology, University of Potsdam.
The study titled, "Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom," was conducted with funding from the United States Department of Energy Genomics Science Program, the National Science Foundation, and the Gordon and Betty Moore Foundation.
About J. Craig Venter Institute
The J. Craig Venter Institute (JCVI) is a not-for-profit research institute in Rockville, Md. and La Jolla, Calif. dedicated to the advancement of the science of genomics; the understanding of its implications for society; and communication of those results to the scientific community, the public, and policymakers. Founded by J. Craig Venter, Ph.D., the JCVI is home to approximately 200 scientists and staff with expertise in human and evolutionary biology, genetics, bioinformatics/informatics, information technology, high-throughput DNA sequencing, genomic and environmental policy research, and public education in science and science policy. The JCVI is a 501(c)(3) organization. For additional information, please visit www.JCVI.org.