About half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B 12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly up-regulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when cocultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3-dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a previously unidentified and likely sizeable link in both the marine carbon and sulfur cycles.
Diatoms are among the most diverse groups of phytoplankton in the ocean. Despite their widely recognized influence on ocean ecosystems and global biogeochemistry, little is known about the impact of this diversity on large-scale processes. Here, we examined the ramifications of between-species diversity by documenting the transcriptional response of three diatoms -Thalassiosira pseudonana, Fragilariopsis cylindrus, and Pseudo-nitzschia multiseries -to the onset of nitrate limitation of growth, a common limiting nutrient in the ocean. The three species shared 5583 clusters of orthologous genes based on OrthoMCL clustering of publically available diatom genomes. These clusters represent 30-54% of the predicted genes in each diatom genome. Less than 5% of genes within these core clusters displayed the same transcriptional responses across species when growth was limited by nitrate availability. Orthologs, such as those involved in nitrogen uptake and assimilation, as well as carbon metabolism, were differently expressed across the three species. The two pennate diatoms, F. cylindrus and P. multiseries, shared 3839 clusters without orthologs in the genome of the centric diatom T. pseudonana. A majority of these pennate-clustered genes, as well as the non-orthologous genes in each species, had minimal annotation information, but were often significantly differentially expressed under nitrate limitation, indicating their potential importance in the response to nitrogen availability. Despite these variations in the specific transcriptional response of each diatom, overall transcriptional patterns suggested that all three diatoms displayed a common physiological response to nitrate limitation that consisted of a general reduction in carbon fixation and carbohydrate and fatty acid metabolism and an increase in nitrogen recycling. Characterization of these finely tuned responses will help to better predict which types of diatoms will bloom under which sets of environmental factors.
In the modern ocean, phytoplankton maintain extremely high primary production/biomass ratios, indicating that they bloom, die, and are replaced weekly. The molecular mechanisms regulating cellular mortality and turnover are largely unknown, even though they effectively short-circuit carbon export to the deep ocean and channel primary productivity to microbial food webs. Here, we present morphological, biochemical, and molecular evidence of caspase-mediated, autocatalytic programmed cell death (PCD) in the diatom Thalassiosira pseudonana in response to iron starvation. Transmission electron microscopy revealed internal degradation of nuclear, chloroplastic, and mitochondrial organelles, all while the plasma membranes remained intact. Cellular degradation was concomitant with dramatic decreases in photosynthetic efficiency, externalization of phosphatidylserine, and significantly elevated caspase-specific activity, with the addition of a broad-spectrum caspase inhibitor rescuing cells from death. A search of the T. pseudonana genome identified six distinct putative metacaspases containing a conserved caspase domain structure. Phytoplankton, or unicellular photoautotrophs that drift with the currents, represent the base of most marine food webs. Although they account for Ͻ1% of the Earth's biomass, they are responsible for nearly 50% of global annual carbonbased primary productivity (31). The steady-state maintenance of such a high production/biomass ratio implies that, on average, these organisms grow, die, and are replaced once every week (57). Substantial cell death via lysis documented in field populations of phytoplankton (1, 2, 14, 16, 58) challenges the long-held misconception among biological oceanographers that phytoplankton are immortal unless eaten by zooplankton grazers and highlights the importance of key death processes to marine ecosystems. Unfortunately, the mechanisms regulating phytoplankton cell death have received relatively little attention, even though they serve to couple primary production to microbial food webs (10), effectively short-circuiting carbon export to the deep ocean and stimulating upper ocean biogeochemical cycling (4, 10).Autocatalytic cell death triggered by specific environmental stresses (e.g., cell age, nutrient deprivation, high light levels, oxidative stress, and UV exposure) in prokaryotic and eukaryotic unicellular phytoplankton (6,10,42,51,59) provides a mechanism to explain the high lysis rates independent of viral attack or grazing. This cellular self destruction is analogous to programmed cell death (PCD) in multicellular organisms, a form of autocatalytic cell suicide in which an endogenous biochemical pathway leads to apoptotic-like morphological changes and, ultimately, cellular dissolution. PCD involves the expression and biochemical coordination of specialized cellular machinery, such as receptors, adaptors, signal kinases, proteases, and nuclear factors. A specific class of intracellular cysteinyl aspartate-specific proteases, termed caspases, is of particular...
Diverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways.
Universal taxonomic frameworks have been critical tools to structure the fields of botany, zoology, mycology, and bacteriology as well as their large research communities. Animals, plants, and fungi have relatively solid, stable morpho‐taxonomies built over the last three centuries, while bacteria have been classified for the last three decades under a coherent molecular taxonomic framework. By contrast, no such common language exists for microbial eukaryotes, even though environmental ‘‐omics’ surveys suggest that protists make up most of the organismal and genetic complexity of our planet's ecosystems! With the current deluge of eukaryotic meta‐omics data, we urgently need to build up a universal eukaryotic taxonomy bridging the protist ‐omics age to the fragile, centuries‐old body of classical knowledge that has effectively linked protist taxa to morphological, physiological, and ecological information. UniEuk is an open, inclusive, community‐based and expert‐driven international initiative to build a flexible, adaptive universal taxonomic framework for eukaryotes. It unites three complementary modules, EukRef, EukBank, and EukMap, which use phylogenetic markers, environmental metabarcoding surveys, and expert knowledge to inform the taxonomic framework. The UniEuk taxonomy is directly implemented in the European Nucleotide Archive at EMBL‐EBI, ensuring its broad use and long‐term preservation as a reference taxonomy for eukaryotes.
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