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The Molecular Life of Diatoms: From Genes to Ecosystems

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A special issue of Biology (ISSN 2079-7737).

Deadline for manuscript submissions: closed (15 April 2020) | Viewed by 37532

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Special Issue Editor

Prof. Dr. Thomas Mock

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Guest Editor

School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR47TJ, UK
Interests: algal genomics; genome editing; phytoplankton; evolution; ecology; adaptation; microbiology

Special Issue Information

Dear Colleagues,

Diatoms are the most species-rich group of algae and contribute about 20% of annual global carbon fixation. They play major roles in ocean food webs and global biogeochemical cycles. They are also a target of the biotechnology industry because of their nano-patterned silica cell wall and high lipid content. Diatoms have received increasing attention as more genomes became available and because of the development of genome-editing tools. CRISPR/Cas9 technology has made diatoms as genetically tractable as well-established biological model species. In this Special Issue, we will bring together diverse contributions from the field of molecular diatom research. Our community is currently experiencing a step change in understanding diatoms from genes to ecosystems. The aim of this Special Issue is to offer a forum for new scientific concepts and ideas in the form of review articles and perspectives in addition to research papers based on the application of molecular tools and genomic information to give examples of the fascinating lifestyle of diatoms and their significance for many different fields of science.

Prof. Thomas Mock
Guest Editor

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Keywords

biotechnology
genome editing
molecular biological oceanography
genomics
evolution
ecology
adaptation
metagenomics
metatranscriptomics

Published Papers (7 papers)

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Research

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25 pages, 2405 KiB

Open AccessFeature PaperArticle

The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom

by Maxine H. Tan, Sarah R. Smith, Kim K. Hixson, Justin Tan, James K. McCarthy, Adam B. Kustka and Andrew E. Allen

Biology 2020, 9(7), 155; https://doi.org/10.3390/biology9070155 - 6 Jul 2020

Cited by 5 | Viewed by 3674

Abstract

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. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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20 pages, 1654 KiB

Open AccessArticle

Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness

by Michel Lavoie, Blanche Saint-Béat, Jan Strauss, Sébastien Guérin, Antoine Allard, Simon V. Hardy, Angela Falciatore and Johann Lavaud

Biology 2020, 9(2), 30; https://doi.org/10.3390/biology9020030 - 17 Feb 2020

Cited by 7 | Viewed by 5209

Abstract

Diatoms are major primary producers in polar environments where they can actively grow under extremely variable conditions. Integrative modeling using a genome-scale model (GSM) is a powerful approach to decipher the complex interactions between components of diatom metabolism and can provide insights into metabolic mechanisms underlying their evolutionary success in polar ecosystems. We developed the first GSM for a polar diatom, Fragilariopsis cylindrus, which enabled us to study its metabolic robustness using sensitivity analysis. We find that the predicted growth rate was robust to changes in all model parameters (i.e., cell biochemical composition) except the carbon uptake rate. Constraints on total cellular carbon buffer the effect of changes in the input parameters on reaction fluxes and growth rate. We also show that single reaction deletion of 20% to 32% of active (nonzero flux) reactions and single gene deletion of 44% to 55% of genes associated with active reactions affected the growth rate, as well as the production fluxes of total protein, lipid, carbohydrate, DNA, RNA, and pigments by less than 1%, which was due to the activation of compensatory reactions (e.g., analogous enzymes and alternative pathways) with more highly connected metabolites involved in the reactions that were robust to deletion. Interestingly, including highly divergent alleles unique for F. cylindrus increased its metabolic robustness to cellular perturbations even more. Overall, our results underscore the high robustness of metabolism in F. cylindrus, a feature that likely helps to maintain cell homeostasis under polar conditions. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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19 pages, 5048 KiB

Open AccessArticle

Metabarcoding Reveals Temporal Patterns of Community Composition and Realized Thermal Niches of Thalassiosira Spp. (Bacillariophyceae) from the Narragansett Bay Long-Term Plankton Time Series

by Tatiana A. Rynearson, Sarah A. Flickinger and Diana N. Fontaine

Biology 2020, 9(1), 19; https://doi.org/10.3390/biology9010019 - 16 Jan 2020

Cited by 20 | Viewed by 4576

Abstract

Diatoms generate nearly half of marine primary production and are comprised of a diverse array of species that are often morphologically cryptic or difficult to identify using light microscopy. Here, species composition and realized thermal niches of species in the diatom genus Thalassiosira were examined at the site of the Narragansett Bay (NBay) Long-Term Plankton Time Series using a combination of light microscopy (LM), high-throughput sequencing (HTS) of the 18S rDNA V4 region and historical records. Thalassiosira species were identified over 6 years using a combination of LM and DNA sequences. Sixteen Thalassiosira taxa were identified using HTS: nine were newly identified in NBay. Several newly identified species have small cell diameters and are difficult to identify using LM. However, they appeared frequently and thus may play a significant ecological role in NBay, particularly since their realized niches suggest they are eurythermal and able to tolerate the >25 °C temperature range of NBay. Four distinct species assemblages that grouped by season were best explained by surface water temperature. When compared to historical records, we found that the cold-water species Thalassiosira nordenskioeldii has decreased in persistence over time, suggesting that increasing surface water temperature has influenced the ecology of phytoplankton in NBay. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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9 pages, 1457 KiB

Open AccessCommunication

Optimizing the Design of Diatom Biosilica-Targeted Fusion Proteins in Biosensor Construction for Bacillus anthracis Detection

by Nicole R. Ford, Yijia Xiong, Karen A. Hecht, Thomas C. Squier, Gregory L. Rorrer and Guritno Roesijadi

Biology 2020, 9(1), 14; https://doi.org/10.3390/biology9010014 - 7 Jan 2020

Cited by 8 | Viewed by 3487

Abstract

In vivo functionalization of diatom biosilica frustules by genetic manipulation requires careful consideration of the overall structure and function of complex fusion proteins. Although we previously had transformed Thalassiosira pseudonana with constructs containing a single domain antibody (sdAb) raised against the Bacillus anthracis Sterne strain, which detected an epitope of the surface layer protein EA1 accessible in lysed spores, we initially were unsuccessful with constructs encoding a similar sdAb that detected an epitope of EA1 accessible in intact spores and vegetative cells. This discrepancy limited the usefulness of the system as an environmental biosensor for B. anthracis. We surmised that to create functional biosilica-localized biosensors with certain constructs, the biosilica targeting and protein trafficking functions of the biosilica-targeting peptide Sil3_T8 had to be uncoupled. We found that retaining the ER trafficking sequence at the N-terminus and relocating the Sil3_T8 targeting peptide to the C-terminus of the fusion protein resulted in successful detection of EA1 with both sdAbs. Homology modeling of antigen binding by the two sdAbs supported the hypothesis that the rescue of antigen binding in the previously dysfunctional sdAb was due to removal of steric hindrances between the antigen binding loops and the diatom biosilica for that particular sdAb. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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Graphical abstract

17 pages, 2400 KiB

Open AccessArticle

Storage Compound Accumulation in Diatoms as Response to Elevated CO₂ Concentration

by Erik L. Jensen, Karen Yangüez, Frédéric Carrière and Brigitte Gontero

Biology 2020, 9(1), 5; https://doi.org/10.3390/biology9010005 - 24 Dec 2019

Cited by 24 | Viewed by 4326

Abstract

Accumulation of reserve compounds (i.e., lipids and chrysolaminarin) in diatoms depends on the environmental conditions, and is often triggered by stress conditions, such as nutrient limitation. Manipulation of CO₂ supply can also be used to improve both lipids and carbohydrates accumulation. Given the high diversity among diatoms, we studied the two marine model diatoms—Thalassiosira pseudonana and Phaeodactylum tricornutum, a freshwater diatom, Asterionella formosa, and Navicula pelliculosa—found in fresh- and sea-water environments. We measured the accumulation of reserve compounds and the activity of enzymes involved in carbon metabolism in these diatoms grown at high and atmospheric CO₂. We observed that biomass and lipid accumulation in cells grown at high CO₂ differ among the diatoms. Lipid accumulation increased only in P. tricornutum and N. pelliculosa grown in seawater in response to elevated CO₂. Moreover, accumulation of lipids was also accompanied by an increased activity of the enzymes tested. However, lipid accumulation and enzyme activity decreased in N. pelliculosa cultured in fresh water. Chrysolaminarin accumulation was also affected by CO₂ concentration; however, there was no clear relation with lipids accumulation. Our results are relevant to understand better the ecological role of the environment in the diatom adaptation to CO₂ and the mechanisms underpinning the production of storage compounds considering diatom diversity. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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Review

Jump to: Research

28 pages, 2006 KiB

Open AccessReview

Diatoms for Carbon Sequestration and Bio-Based Manufacturing

by Deepak Sethi, Thomas O. Butler, Faqih Shuhaili and Seetharaman Vaidyanathan

Biology 2020, 9(8), 217; https://doi.org/10.3390/biology9080217 - 10 Aug 2020

Cited by 27 | Viewed by 8292

Abstract

Carbon dioxide (CO₂) is a major greenhouse gas responsible for climate change. Diatoms, a natural sink of atmospheric CO₂, can be cultivated industrially in autotrophic and mixotrophic modes for the purpose of CO₂ sequestration. In addition, the metabolic diversity exhibited by this group of photosynthetic organisms provides avenues to redirect the captured carbon into products of value. These include lipids, omega-3 fatty acids, pigments, antioxidants, exopolysaccharides, sulphated polysaccharides, and other valuable metabolites that can be produced in environmentally sustainable bio-manufacturing processes. To realize the potential of diatoms, expansion of our knowledge of carbon supply, CO₂ uptake and fixation by these organisms, in conjunction with ways to enhance metabolic routing of the fixed carbon to products of value is required. In this review, current knowledge is explored, with an evaluation of the potential of diatoms for carbon capture and bio-based manufacturing. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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23 pages, 1157 KiB

Open AccessReview

A Review of Diatom Lipid Droplets

by Ben Leyland, Sammy Boussiba and Inna Khozin-Goldberg

Biology 2020, 9(2), 38; https://doi.org/10.3390/biology9020038 - 21 Feb 2020

Cited by 31 | Viewed by 6093

Abstract

The dynamic nutrient availability and photon flux density of diatom habitats necessitate buffering capabilities in order to maintain metabolic homeostasis. This is accomplished by the biosynthesis and turnover of storage lipids, which are sequestered in lipid droplets (LDs). LDs are an organelle conserved among eukaryotes, composed of a neutral lipid core surrounded by a polar lipid monolayer. LDs shield the intracellular environment from the accumulation of hydrophobic compounds and function as a carbon and electron sink. These functions are implemented by interconnections with other intracellular systems, including photosynthesis and autophagy. Since diatom lipid production may be a promising objective for biotechnological exploitation, a deeper understanding of LDs may offer targets for metabolic engineering. In this review, we provide an overview of diatom LD biology and biotechnological potential. Full article

(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)

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