Mitochondrial fatty acid β-oxidation is required for storage-lipid catabolism in a marine diatom
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Plant Sciences↗
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Declines in ice cover are accompanied by light limitation responses and community change in freshwater diatoms
The rediscovery of diatom blooms embedded within and beneath the Lake Erie ice cover (2007–2012) ignited interest in psychrophilic adaptations and winter limnology. Subsequent studies determined the vital role ice plays in winter diatom ecophysiology as diatoms partition to the underside of ice, thereby fixing their location within the photic zone. Yet, climate change has led to widespread ice decline across the Great Lakes, with Lake Erie presenting a nearly “ice-free” state in several recent winters. It has been hypothesized that the resultant turbid, isothermal water column induces light limitation amongst winter diatoms and thus serves as a competitive disadvantage. To investigate this hypothesis, we conducted a physiochemical and metatranscriptomic survey that spanned spatial, temporal, and climatic gradients of the winter Lake Erie water column (2019–2020). Our results suggest that ice-free conditions decreased planktonic diatom bloom magnitude and altered diatom community composition. Diatoms increased their expression of various photosynthetic genes and iron transporters, which suggests that the diatoms are attempting to increase their quantity of photosystems and light-harvesting components (a well-defined indicator of light limitation). We identified two gene families which serve to increase diatom fitness in the turbid ice-free water column: proton-pumping rhodopsins (a potential second means of light-driven energy acquisition) and fasciclins (a means to “raft” together to increase buoyancy and co-locate to the surface to optimize light acquisition). With large-scale climatic changes already underway, our observations provide insight into how diatoms respond to the dynamic ice conditions of today and shed light on how they will fare in a climatically altered tomorrow.
54 ENVIRONMENTAL SCIENCES↗
Diatom influence on the production characteristics of hydrate-bearing sediments: Examples from Ulleung Basin, offshore South Korea
The Ulleung Basin Gas Hydrate field expeditions in 2007 (UBGH1) and 2010 (UBGH2) sought to assess the Basin's gas hydrate resource potential. Coring operations in both expeditions recovered evidence of gas hydrate, primarily as fracture-filling (or vein type) morphologies in mainly silt-sized, fine-grained sediment, but also as pore-occupying hydrate in the coarser-grained layers of interbedded sand and fine-grained systems. A commonality across many of these occurrences is the presence of diatoms in the fine-grained sediment. Here we tested fine-grained sediment (median grain size <12.5 μm) associated with hydrate occurrences at four UBGH2 sites (UBGH2-2-2, UBGH2-3, UBGH2-6 and UBGH2-11) to investigate potential impacts of diatoms on efforts to extract methane from hydrate, or to tap hydrocarbon reservoirs beneath hydrate-bearing sediment. Two key considerations are: the extent to which diatoms control sediment mechanical properties, and the extent to which pore-water freshening, which occurs as gas hydrate breaks down during resource extraction, alters the diatom control on sediment mechanical properties. We conducted experiments to measure sediment index properties, sedimentation behavior and compressibility to address these considerations. We relied on scanning electron microscope (SEM) imagery and X-ray powder diffraction (XRD) to characterize the sediment mineralogy. Our high-level findings are that at the ~20–45% (by volume) diatom concentrations observed at these UBGH2 sites, sediment compressibility increases with diatom content, but diatoms only appear to increase porosity and permeability at the highest diatom concentration (~45%). Our measurements suggest in situ compression indices of 0.35–0.55 and permeabilities on the order of 0.01milliDarcies (1 × 10 -17 m 2 ) can be anticipated at these sites. Importantly, these properties are not expected to vary significantly upon pore water freshening that accompanies gas hydrate dissociation during production.
58 GEOSCIENCES↗
Revealing the Bacterial Quorum-Sensing Effect on the Biofilm Formation of Diatom Cylindrotheca sp. Using Multimodal Imaging
Diatoms contribute to carbon fixation in the oceans by photosynthesis and always form biofouling organized by extracellular polymeric substances (EPS) in the marine environment. Bacteria-produced quorum-sensing signal molecules N-acyl homoserine lactones (AHLs) were found to play an important role in the development of Cylindrotheca sp. in previous studies, but the EPS composition change was unclear. This study used the technology of alcian blue staining and scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM), and time-of-flight secondary ion mass spectrometry (ToF-SIMS) to directly observe the biofilm formation process. The results showed that AHLs promote the growth rates of diatoms and the EPS secretion of biofilm components. AHLs facilitated the diatom-biofilm formation by a forming process dependent on the length of carbon chains. AHLs increased the biofilm thickness and the fluorescence intensity and then altered the three-dimensional (3D) structures of the diatom-biofilm. In addition, the enhanced EPS content in the diatom-biofilm testified that AHLs aided biofilm formation. This study provides a collection of new experimental evidence of the interaction between bacteria and microalgae in fouling biofilms.
59 BASIC BIOLOGICAL SCIENCES↗
Design of Ru-Ni diatomic sites for efficient alkaline hydrogen oxidation
Anion exchange membrane fuel cells are limited by the slow kinetics of alkaline hydrogen oxidation reaction (HOR). Here, we establish HOR catalytic activities of single-atom and diatomic sites as a function of *H and *OH binding energies to screen the optimal active sites for the HOR. As a result, the Ru-Ni diatomic one is identified as the best active center. Guided by the theoretical finding, we subsequently synthesize a catalyst with Ru-Ni diatomic sites supported on N-doped porous carbon, which exhibits excellent catalytic activity, CO tolerance, and stability for alkaline HOR and is also superior to single-site counterparts. In situ scanning electrochemical microscopy study validates the HOR activity resulting from the Ru-Ni diatomic sites. Furthermore, in situ x-ray absorption spectroscopy and computational studies unveil a synergistic interaction between Ru and Ni to promote the molecular H 2 dissociation and strengthen OH adsorption at the diatomic sites, and thus enhance the kinetics of HOR.
25 ENERGY STORAGE↗
A re-examination of the mechanism of whiting events: A new role for diatoms in Fayetteville Green Lake (New York, USA)
Whiting events—the episodic precipitation of fine-grained suspended calcium carbonates in the water column—have been documented across a variety of marine and lacustrine environments. Whitings likely are a major source of carbonate muds, a constituent of limestones, and important archives for geochemical proxies of Earth history. While several biological and physical mechanisms have been proposed to explain the onset of these precipitation events, no consensus has been reached thus far. Fayetteville Green Lake (New York, USA) is a meromictic lake that experiences annual whitings. Materials suspended in the water column collected through the whiting season were characterized using scanning electron microscopy and scanning transmission X-ray microscopy. Whitings in Fayetteville Green Lake are initiated in the spring within the top few meters of the water column, by precipitation of fine amorphous calcium carbonate (ACC) phases nucleating on microbial cells, as well as on abundant extracellular polymeric substances (EPS) frequently associated with centric diatoms. Whiting particles found in the summer consist of 5–7 μm calcite grains forming aggregates with diatoms and EPS. Simple calculations demonstrate that calcite particles continuously grow over several days, then sink quickly through the water column. In the late summer, partial calcium carbonate dissolution is observed deeper in the water column. Settling whiting particles, however, reach the bottom of the lake, where they form a major constituent of the sediment, along with diatom frustules. The role of diatoms and associated EPS acting as nucleation surfaces for calcium carbonates is described for the first time here as a potential mechanism participating in whitings at Fayetteville Green Lake. This mechanism may have been largely overlooked in other whiting events in modern and ancient environments.
54 ENVIRONMENTAL SCIENCES↗
The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom
Diatoms are major contributors to global primary production and their populations in the modern oceans are affected by availability of iron, nitrogen, phosphate, silica, and other trace metals, vitamins, and infochemicals. However, little is known about the role of phosphorylation in diatoms and its role in regulation and signaling. We report a total of 2759 phosphorylation sites on 1502 proteins detected in Phaeodactylum tricornutum. Conditionally phosphorylated peptides were detected at low iron (n = 108), during the diel cycle (n = 149), and due to nitrogen availability (n = 137). Through a multi-omic comparison of transcript, protein, phosphorylation, and protein homology, we identify numerous proteins and key cellular processes that are likely under control of phospho-regulation. We show that phosphorylation regulates: (1) carbon retrenchment and reallocation during growth under low iron, (2) carbon flux towards lipid biosynthesis after the lights turn on, (3) coordination of transcription and translation over the diel cycle and (4) in response to nitrogen depletion. We also uncover phosphorylation sites for proteins that play major roles in diatom Fe sensing and utilization, including flavodoxin and phytotransferrin (ISIP2A), as well as identify phospho-regulated stress proteins and kinases. These findings provide much needed insight into the roles of protein phosphorylation in diel cycling and nutrient sensing in diatoms.
59 BASIC BIOLOGICAL SCIENCES↗
Non-Invasive Biophysical Techniques to Monitor the Structural Plasticity of the Photosynthetic Machinery of Live Diatom Cells
The photosynthetic performance of diatoms depends largely on the organization and structural flexibility of their thylakoid membranes, the densely packed, highly organized membrane vesicles in which light reactions of photosynthesis occur. Different regulatory mechanisms that fine tune the photosynthetic functions affect the organization of the photosynthetic machinery at different levels of structural complexity, from the level of individual protein complexes to the macroarray of membrane proteins and the remodeling of the entire thylakoid membrane system. To monitor these reorganizations, non-invasive techniques are of special value. In this chapter, we focus our attention on three of these techniques, which have been demonstrated to provide unique and useful information on the structure and structural and functional plasticity of live diatom cells: (i) circular dichroism (CD) spectroscopy, which has provided unique information on the chiral (macro-)organization of protein complexes and on their rapid, reversible reorganizations, fine-tuning the light-harvesting processes, as well as on variations in the short-range excitonic interactions in the antenna complexes; (ii) small-angle neutron scattering (SANS), which has been used to determine the periodic organization of the thylakoid membranes and to monitor reversible ultrastructural changes on the time-scale of minutes, induced by variations in the environmental conditions such as changes in temperature or light intensity; and (iii) electrochromic shift absorbance transients (ΔA ECS ), a spectroscopic tool which has been shown to be capable of identifying distinct functional groups of the light-harvesting carotenoid fucoxanthin in different diatoms and in cells exposed to different light intensities. Future use of these techniques will most certainly contribute to the deeper understanding of key regulatory mechanisms of photosynthesis in diatoms.
Szabo, Milan↗
Adaptive responses of marine diatoms to zinc scarcity and ecological implications
Scarce dissolved surface ocean concentrations of the essential algal micronutrient zinc suggest that Zn may influence the growth of phytoplankton such as diatoms, which are major contributors to marine primary productivity. However, the specific mechanisms by which diatoms acclimate to Zn deficiency are poorly understood. Using global proteomic analysis, we identified two proteins (ZCRP-A/B, Zn/Co Responsive Protein A/B) among four diatom species that became abundant under Zn/Co limitation. Characterization using reverse genetic techniques and homology data suggests putative Zn/Co chaperone and membrane-bound transport complex component roles for ZCRP-A (a COG0523 domain protein) and ZCRP-B, respectively. Metaproteomic detection of ZCRPs along a Pacific Ocean transect revealed increased abundances at the surface (<200 m) where dZn and dCo were scarcest, implying Zn nutritional stress in marine algae is more prevalent than previously recognized. These results demonstrate multiple adaptive responses to Zn scarcity in marine diatoms that are deployed in low Zn regions of the Pacific Ocean.
54 ENVIRONMENTAL SCIENCES↗
A charged diatomic triple-bonded U≡N species trapped in C 82 fullerene cages
Actinide diatomic molecules are ideal models to study elusive actinide multiple bonds, but most of these diatomic molecules have so far only been studied in solid inert gas matrices. Herein, we report a charged U≡N diatomic species captured in fullerene cages and stabilized by the U-fullerene coordination interaction. Two diatomic clusterfullerenes, viz. UN@C s (6)-C 82 and UN@C 2 (5)-C 82 , were successfully synthesized and characterized. Crystallographic analysis reveals U-N bond lengths of 1.760(7) and 1.760(20) Å in UN@C s (6)-C 82 and UN@C 2 (5)-C 82 . Moreover, U≡N was found to be immobilized and coordinated to the fullerene cages at 100 K but it rotates inside the cage at 273 K. Quantum-chemical calculations show a (UN) 2+ @(C 82 ) 2- electronic structure with formal +5 oxidation state (f 1 ) of U and unambiguously demonstrate the presence of a U≡N bond in the clusterfullerenes. This study constitutes an approach to stabilize fundamentally important actinide multiply bonded species.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Diploid genomic architecture of Nitzschia inconspicua, an elite biomass production diatom
Abstract A near-complete diploid nuclear genome and accompanying circular mitochondrial and chloroplast genomes have been assembled from the elite commercial diatom species Nitzschia inconspicua . The 50 Mbp haploid size of the nuclear genome is nearly double that of model diatom Phaeodactylum tricornutum , but 30% smaller than closer relative Fragilariopsis cylindrus . Diploid assembly, which was facilitated by low levels of allelic heterozygosity (2.7%), included 14 candidate chromosome pairs composed of long, syntenic contigs, covering 93% of the total assembly. Telomeric ends were capped with an unusual 12-mer, G-rich, degenerate repeat sequence. Predicted proteins were highly enriched in strain-specific marker domains associated with cell-surface adhesion, biofilm formation, and raphe system gliding motility. Expanded species-specific families of carbonic anhydrases suggest potential enhancement of carbon concentration efficiency, and duplicated glycolysis and fatty acid synthesis pathways across cytosolic and organellar compartments may enhance peak metabolic output, contributing to competitive success over other organisms in mixed cultures. The N. inconspicua genome delivers a robust new reference for future functional and transcriptomic studies to illuminate the physiology of benthic pennate diatoms and harness their unique adaptations to support commercial algae biomass and bioproduct production.
09 BIOMASS FUELS↗
Spin-free formulation of the multireference driven similarity renormalization group: A benchmark study of first-row diatomic molecules and spin-crossover energetics
We report a spin-free formulation of the multireference (MR) driven similarity renormalization group (DSRG) based on the ensemble normal ordering of Mukherjee and Kutzelnigg (1997). This ensemble averages over all microstates of a given total spin quantum number, and therefore, it is invariant with respect to SU(2) transformations. As such, all equations may be reformulated in terms of spin-free quantities and they closely resemble those of spin-adapted closed-shell coupled cluster (CC) theory. The current implementation is used to assess the accuracy of various truncated MR-DSRG methods (perturbation theory up to third order and iterative methods with single and double excitations) in computing the constants of 33 first-row diatomic molecules. The accuracy trends for these first-row diatomics are consistent with our previous benchmark on a small subset of closed-shell diatomic molecules. We then present the first MR-DSRG application on transition-metal complexes by computing the spin splittings of the [Fe(H 2 O) 6 ] 2+ and [Fe(NH 3 ) 6 ] 2+ molecules. A focal point analysis (FPA) shows that third-order perturbative corrections are essential to achieve reasonably converged energetics. The FPA based on the linearized MR-DSRG theory with one- and two-body operators and up to a quintuple- ζ basis set predicts the spin splittings of [Fe(H 2 O) 6 ] 2+ and [Fe(NH 3 ) 6 ] 2+ to be –35.7 and –17.1 kcal mol –1 , respectively, showing good agreement with the results of local CC theory with singles, doubles, and perturbative triples.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Green diatom mutants reveal an intricate biosynthetic pathway of fucoxanthin
Fucoxanthin is a major light-harvesting pigment in ecologically important algae such as diatoms, haptophytes, and brown algae (Phaeophyceae). Therefore, it is a major driver of global primary productivity. Species of these algal groups are brown colored because the high amounts of fucoxanthin bound to the proteins of their photosynthetic machineries enable efficient absorption of green light. While the structure of these fucoxanthin-chlorophyll proteins has recently been resolved, the biosynthetic pathway of fucoxanthin is still unknown. Here, we identified two enzymes central to this pathway by generating corresponding knockout mutants of the diatom Phaeodactylum tricornutum that are green due to the lack of fucoxanthin. Complementation of the mutants with the native genes or orthologs from haptophytes restored fucoxanthin biosynthesis. We propose a complete biosynthetic path to fucoxanthin in diatoms and haptophytes based on the carotenoid intermediates identified in the mutants and in vitro biochemical assays. It is substantially more complex than anticipated and reveals diadinoxanthin metabolism as the central regulatory hub connecting the photoprotective xanthophyll cycle and the formation of fucoxanthin. Moreover, our data show that the pathway evolved by repeated duplication and neofunctionalization of genes for the xanthophyll cycle enzymes violaxanthin de-epoxidase and zeaxanthin epoxidase. Brown algae lack diadinoxanthin and the genes described here and instead use an alternative pathway predicted to involve fewer enzymes. Our work represents a major step forward in elucidating the biosynthesis of fucoxanthin and understanding the evolution, biogenesis, and regulation of the photosynthetic machinery in algae.
59 BASIC BIOLOGICAL SCIENCES↗
Probing Nanoscale Chemical Environments of Zinc in Diatoms
Diatoms impact the biogeochemical cycling of zinc (Zn) due to elevated cellular Zn levels over other phytoplankton, and their strong biological uptake of Zn in the Southern Ocean sets the global distribution of Zn in ocean water columns. Past studies have revealed the abundance and spatial distribution of Zn in individual diatoms, while others have shown diverse Zn chemical species in whole-cell aggregates. However, intracellular and intercellular variations in Zn chemical forms remained unknown. For the first time, we applied a synchrotron X-ray nanoprobe to cultured diatoms (Phaeodactylum tricornutum and Chaetoceros muelleri) and resolved spatial heterogeneities of Zn chemistry. The result shows the partitioning of Zn between intracellular contents (soft parts) and frustules (mainly in the intracellular contents for P. tricornutum and similar Zn concentrations in the intracellular contents and frustules for C. muelleri). We found multiple Zn chemical species unevenly distributed within individual cells, where Zn–phosphoryl complexes were the most abundant followed by cysteine, histidine, biogenic silica, and carboxyl complexes. Cellular Zn species varied between individual organisms and were influenced by Zn availability. To our knowledge, this work presents the first X-ray measurements of trace metal speciation at sub-100 nm resolution in biological samples in their natural state. In conclusion, this research improves our ability to examine the biogeochemistry of Zn on the nanoscale and can help us understand the role of Zn in plankton growth and the Zn cycle in ocean waters.
36 MATERIALS SCIENCE↗
Synergistic Effect of Diatomic Mo-B Site Confined in Graphene-Like C 2 N Enables Electrocatalytic Nitrogen Reduction via Novel Mechanism
Structural modulation of active site with atomic-level precision is of great importance to meet the activity and selectivity challenges that electrocatalysts are commonly facing. In this work, we have designed a metal (M) - nonmetal (NM) diatomic site embedded in graphene-like C 2 N (denoted as Mo-B@C 2 N), where electrocatalytic N 2 reduction reaction (eNRR) was thoroughly explored using density functional theory combined with computational hydrogen electrode method. Compared to M-M diatomic sites, Mo-B site can generate pronounced synergistic effect that led to eNRR proceeding via a novel quasi-dissociative reaction mechanism that has not been reported relative to the conventional enzymatic, consecutive, distal, and alternating associative mechanism. This newly uncovered mechanism in which N-N bond scission takes place immediately after the first proton-coupled electron transfer (PCET) step (i.e., *NH-*N + H + + e – ® *NH 2 *N) has demonstrated much advantage in PCET process over the four conventional mechanism in terms of thermodynamic barrier, except that the adsorption of side-on *N 2 seemed thermodynamically unfavorable (DG ads = 0.61eV). Our results have revealed that the activation of inert NºN triple bond is dominated by π*-backdonation mechanism as a consequence of charge transfers from both B and Mo site, and unexpectedly, from the substrate C 2 N itself as well. Moreover, the hybrid Mo-B diatomic site demonstrated superior performance over either Mo-Mo or B-B site for driving eNRR. Furthermore, our study could provide insight into the delicate relationships among atomic site, substrate and electrocatalytic performance.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
A bloom of a single bacterium shapes the microbiome during outdoor diatom cultivation collapse
Algae-dominated ecosystems are fundamentally influenced by their microbiome. We lack information on the identity and function of bacteria that specialize in consuming algal-derived dissolved organic matter in high algal density ecosystems such as outdoor algal ponds used for biofuel production. Here, we describe the metagenomic and metaproteomic signatures of a single bacterial strain that bloomed during a population-wide crash of the diatom, Phaeodactylum tricornutum, grown in outdoor ponds. 16S rRNA gene data indicated that a single Kordia sp. strain (family Flavobacteriaceae) contributed up to 93% of the bacterial community during P. tricornutum demise. Kordia sp. expressed proteins linked to microbial antagonism and biopolymer breakdown, which likely contributed to its dominance over other microbial taxa during diatom demise. Analysis of accompanying downstream microbiota (primarily of the Rhodobacteraceae family) provided evidence that cross-feeding may be a pathway supporting microbial diversity during diatom demise. In situ and laboratory data with a different strain suggested that Kordia was a primary degrader of biopolymers during algal demise, and co-occurring Rhodobacteraceae exploited degradation molecules for carbon. An analysis of 30 Rhodobacteraceae metagenome assembled genomes suggested that algal pond Rhodobacteraceae commonly harbored pathways to use diverse carbon and energy sources, including carbon monoxide, which may have contributed to the prevalence of this taxonomic group within the ponds. These observations further constrain the roles of functionally distinct heterotrophic bacteria in algal microbiomes, demonstrating how a single dominant bacterium, specialized in processing senescing or dead algal biomass, shapes the microbial community of outdoor algal biofuel ponds.
Kordia↗
The diatom Fragilariopsis cylindrus : A model alga to understand cold-adapted life
Diatoms are significant primary producers especially in cold, turbulent, and nutrient-rich surface oceans. Hence, they are abundant in polar oceans, but also underpin most of the polar food webs and related biogeochemical cycles. The cold-adapted pennate diatom Fragilariopsis cylindrus is considered a keystone species in polar oceans and sea ice because it can thrive under different environmental conditions if temperatures are low. In this perspective paper, we provide insights into the latest molecular work that has been done on F. cylindrus and discuss its role as a model alga to understand cold-adapted life.
59 BASIC BIOLOGICAL SCIENCES↗
Multiplexed Knockouts in the Model Diatom Phaeodactylum by Episomal Delivery of a Selectable Cas9
Marine diatoms are eukaryotic microalgae that play significant ecological and biogeochemical roles in oceans. They also have significant potential as organismal platforms for exploitation to address biotechnological and industrial goals. In order to address both modes of research, sophisticated molecular and genetic tools are required. We presented here new and improved methodologies for introducing CRISPRCas9 to the model diatom Phaeodactylum tricornutum cells and a streamlined protocol for genotyping mutant cell lines with previously unknown phenotypes. First, bacterialconjugation was optimized for the delivery of Cas9 by transcriptionally fusing Cas9 to a selectable marker by the 2A peptide. An episome cloning strategy using both negative and positive selection was developed to streamline CRISPR-episome assembly. Next, cell line picking and genotyping strategies, that utilize manual sequencing curation, TIDE sequencing analysis, and a T7 endonuclease assay, were developed to shorten the time required to generate mutants. Following this new experimental pipeline, both singlegene and two-gene knockout cell lines were generated at mutagenesis efficiencies of 48% and 25%, respectively. Lastly, a protocol for precise gene insertions via CRISPRCas9 targeting was developed using particle-bombardment transformation methods. Overall, the novel Cas9 episome design and improved genotyping methods presented here allow for quick and easy genotyping and isolation of Phaeodactylum mutant cell lines (less than 3 weeks) without relying on a known phenotype to screen for mutants.
59 BASIC BIOLOGICAL SCIENCES↗