What Was Old Is New Again: The Pennate Diatom Haslea ostrearia (Gaillon) Simonsen in the Multi-Omic Age

Abstract

The marine pennate diatom Haslea ostrearia has long been known for its characteristic blue pigment marennine, which is responsible for the greening of invertebrate gills, a natural phenomenon of great importance for the oyster industry. For two centuries, this taxon was considered unique; however, the recent description of a new blue Haslea species revealed unsuspected biodiversity. Marennine-like pigments are natural blue dyes that display various biological activities-e.g., antibacterial, antioxidant and antiproliferative-with a great potential for applications in the food, feed, cosmetic and health industries. Regarding fundamental prospects, researchers use model organisms as standards to study cellular and physiological processes in other organisms, and there is a growing and crucial need for more, new and unconventional model organisms to better correspond to the diversity of the tree of life. The present work, thus, advocates for establishing H. ostrearia as a new model organism by presenting its pros and cons-i.e., the interesting aspects of this peculiar diatom (representative of benthic-epiphytic phytoplankton, with original behavior and chemodiversity, controlled sexual reproduction, fundamental and applied-oriented importance, reference genome, and transcriptome will soon be available); it will also present the difficulties encountered before this becomes a reality as it is for other diatom models (the genetics of the species in its infancy, the transformation feasibility to be explored, the routine methods needed to cryopreserve strains of interest).

Keywords: HBIs; Haslea ostrearia; auxosporulation; diatoms; epigenetics; genomics; marennine; phylogeny; transcriptome.

Figure 1

Living cell of Haslea ostrearia (NCC 527) observed in light microscopy.

Figure 2

Molecular phylogeny of 22 species from genera Haslea, Navicula and Gyrosigma based on rbcL gene (1065 bp). The evolutionary history was inferred using the Maximum Likelihood method and General Time Reversible model (test of phylogeny: bootstrap, 1000). Multiple alignment of sequences was carried out using MAFFT [51]. Phylogeny analysis was conducted in PHYML [52].

Figure 3

Flowchart of the bioinformatic pipeline used to assemble the HoB4 genome.

Figure 4

Krona plot of the microbiome detected by searching 16S amplicons in HoB4 metagenomic assembly. The plot displays relative abundance and hierarchy with the use of a radial space-filling display. The amplicons were searched with primers targeting the V1-V3 region of the 16S rRNA gene [90]. The taxonomy was assigned using Qiime2 2021.2.0 and the Silva database 132_99_16S [91,92] and the krona plot was made using KronaTools 2.7.1 [93]. The relative abundance was estimated using the mean depth associated with the bacterial contigs.

Figure 5

Methylation pathway by DNMTs (DNA methyltransferases) and demethylation by TET (ten-eleven translocation) proteins. The latter will oxidize 5mC to 5hmC (5-hydromethylcytosine). Several oxidations via the TET proteins lead to the formation of 5fC (5-formylcytosine) and 5 caC (5-carboxylcytosine). TDG (thymine DNA glycosylase) allows the excision of these last two bases and the return to an unmethylated cytosine. Figure adapted from [103].

Figure 6

Results of ELISA tests performed using H. ostrearia exposed to (a,b) ultraviolet (UV) stress or (c,d) diuron treatments. In both conditions, cells were grown under 100 µmol photons m⁻² s⁻¹, and under 14 h/10 h L/D cycles. The 2 h UV radiation (UVR) stress consisted of UVB (450 mW m⁻²) + UVA (11 W m⁻²) exposition. Diuron was used at different concentrations (0; 5 and 10 µg/L). Graphs 5mC and 5hmC correspond to the ELISA assay quantifying the global level of C-methylation and active demethylation of the genome, respectively.

Figure 7

In situ blue Haslea species blooms, observed in natural environments in (a,c) the Mediterranean Sea (Calvi, Corsica, France), (b) the Adriatic Sea (Dubrovnick, Croatia, B), and (d) the Atlantic Ocean (Morehead City, NC, USA).

Figure 8

Molecular biomarkers involved in the defense of cellular mechanisms characterized in Haslea ostrearia HoB4.

Figure 9

Structure of different terpenoids produced by diatoms: (a) carotenoids; (b) sterols; and (c) highly branched isoprenoids. Figure adapted from [143].

Figure 10

(a) GC-MS chromatogram of the non-saponifiable hexane extract of Haslea HoB4 strain and mass spectrum of the major HBI detected; (b) ¹H NMR spectrum of the C₂₅ tetraene (E)-2,6,14-trimethyl-10-methylene-9-(3-methylpent-4-en-1-yl)pentadeca-2,6-diene isolated after HPLC purification.

Figure 11

Generation of functional oligomers from natural rubber, grafting on model silica particles and on frustule surfaces, and preparation of charged elastic films.

Figure 12

Mesoporous silica particles: (top) before grafting triethoxysilane oligoisoprene; (bottom) after grating triethoxysilane oligoisoprene. Haslea frustules: (top) after elimination of organic matter; (bottom) after grafting triethoxysilane oligoisoprene. TEM micrographs (from JEOL JEM 2100HR, LaB6, 200 KV£). * Specific surface from BET measurements.

Figure 13

UV–Vis spectra of marennine (Mn) and the effect of trimethylamine (TMA) on its color, monitored for 120 min.

Figure 14

Cyclic voltammetry recorded at 100 mV·s⁻¹ on a polished glassy-carbon electrode in a phosphate buffer solution (pH 4) containing the marennine acidolysis product (0.5 mg·mL⁻¹).