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Chitin Synthase Localization in the Diatom Thalassiosira Pseudonana Martin Wustmann1, Nicole Poulsen2, Nils Kröger2,3,4 and Karl‑Heinz Van Pée1*

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Chitin Synthase Localization in the Diatom Thalassiosira Pseudonana Martin Wustmann1, Nicole Poulsen2, Nils Kröger2,3,4 and Karl‑Heinz Van Pée1* Wustmann et al. BMC Mat (2020) 2:10 https://doi.org/10.1186/s42833-020-00016-9 BMC Materials RESEARCH ARTICLE Open Access Chitin synthase localization in the diatom Thalassiosira pseudonana Martin Wustmann1, Nicole Poulsen2, Nils Kröger2,3,4 and Karl‑Heinz van Pée1* Abstract Chitin constitutes an abundant component in many biologically formed minerals (biominerals). While the role of chi‑ tin for the formation and properties of calcium‑based biominerals has been extensively studied, little is known about its role in silica‑based biominerals. Furthermore, there is hardly any information about the enzyme machinery for chitin biosynthesis in biomineral‑forming organisms. Here we have identifed a chitin synthase, chs7305, in the diatom Thalassiosira pseudonana. In stationary cells, chs7305 is located specifcally in a ring pattern in the region of the silici‑ fed girdle bands. The expression pattern of the chs7305 gene and the co‑localization of the encoded enzyme with chitin provides evidence for the importance of chitin synthesis for cell wall function under nutrient limited conditions. Chs7305 is the frst chitin synthase that has been localized in a diatom. Keywords: Chitin, Chitin synthase, Thalassiosira pseudonana, Peptide antibody, Immunolocalization Introduction to high impact resistance and is believed to infuence Diatoms are outstanding examples of unicellular organ- the process of biomineralization [13, 14]. In some cen- isms capable of forming complex shaped cell walls made tric diatoms, chitin is present as crystalline β-chitin fb- of silica [1, 2]. Te silica building blocks of the cell wall ers that are extruded through specialized openings in are produced in a yet little understood morphogenetic the cell wall called fultoportulae. Tese chitin fbers are process that is believed to involve long chain polyam- not involved in silica biomineralization, and instead are ines (LCPA), unique families of proteins (e.g., silafns, believed to slow-down the sinking rate of the photosyn- silacidins), and insoluble organic matrices [3, 4]. Tree thetically active diatom cells by increasing their drag in types of insoluble organic matrices were recently identi- the water [15–17]. Distinct from the chitin fbers are the fed as integral components of the silica cell wall of the chitin meshworks, which are tightly associated with the diatom Talassiosira pseudonana: meshworks [5], micro- silica of the cell wall (rather than being extruded) sug- rings [6] and microplates [7]. Te meshworks are chitin- gesting a possible involvement in silica biogenesis [5, 18]. based with proteins as minor components, whereas the Potential chitin synthase genes seem to be widely dis- microrings and microplates are mainly composed of tributed among diatoms and can even be found in spe- proteins [5–7]. Many diferent organisms employ insolu- cies not known to produce extracellular chitin fbers [18]. ble organic matrices as central components for the bio- T. pseudonana possess four potential chitin synthase synthesis of mineralized structures (biomineralization) genes [18, 19], which is consistent with the need to pro- [8]. Te presence of chitin is particularly well studied in duce at least two diferent types of chitin, secreted fbers CaCO3 biomineralization [8–12]. In nacre it contributes and silica-associated meshworks. Based on the amino acid sequence, it is impossible to predict which chitin synthase produces which type of chitin. To obtain infor- *Correspondence: karl‑[email protected]‑dresden.de 1 General Biochemistry, Technical University of Dresden, 01062 Dresden, mation of the chitin synthases, we attempted the localiza- Germany tion of the enzymes. Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wustmann et al. BMC Mat (2020) 2:10 Page 2 of 7 We chose to focus our studies on chitin synthase 7305 Peptide antibody production and specifcity tests (chs7305, JGI-ID: 7305), because it is predicted to contain Peptide synthesis and subsequent immunization of a myosin motor-like domain, which would indicate an rabbits was conducted by (Davids Biotechnologie intimate association of this chitin synthase with the actin (Regensburg, Germany). Te peptide SEELQSTDKV- cytoskeleton [18]. Actin has previously been found asso- CAQMTDEDKK was used as the target epitope region of ciated with the silica forming organelles of diatoms, the chs7305. Te antibody was afnity-purifed by the manu- silica deposition vesicles (SDVs), and was hypothesized facturer and the specifcity was tested as follows. First, to infuence silica biogenesis through yet unidentifed in a peptide competition assay (PCA), the synthesized transmembrane proteins in the SDV [4]. Furthermore, a peptide was pre-incubated at 10- and 100-times excess chitin synthase from the mussel Mytilus galloprovincialis with anti-chs7305 for 1 h at 23 °C. Te solution was then that also contains a predicted myosin motor domain was used for immunolocalization as described below. Sec- shown to be located in the developing shell, and was sug- ond, the IgG fraction from pre-immune serum was iso- gested to function in in the mineral biogenesis process lated by G-Mag-Sepharose (GE Healthcare, Heidelberg, [12]. Germany) according to the manufacturer’s recommen- dations. Tis IgG fraction was subsequently used for the immunolocalization at the same protein concentration as Methods anti-chs7305. Cultivation T. pseudonana (CCMP1335) was grown in enriched arti- fcial seawater medium according to the recipe of the Immunofuorescence microscopy North East Pacifc Culture Collection [20] at 18 °C under Cells were harvested after 10 days of growth and the constant light (4000–7000 lx). immunolabelling was carried out in 50 mM Tris-bufered saline (TBS, pH 7.5). After a single washing step, the cells Cloning and expression of recombinant proteins in T. were fxed in 2% formaldehyde for 2 h (23 °C, 0.1% Triton pseudonana X-100). Subsequently, the cells were thoroughly washed Te expression of chs7305 was done using the expression and permeabilized in 1.5% Triton X-100 (1% BSA). Te vector pTpNR/egfp which provides a switchable expres- pellet was again thoroughly washed followed by a block- sion [21]. Te chs7305 gene or gene fragments were ing step with a 1% BSA solution. Te incubation with amplifed from genomic DNA with the oligonucleotides the primary antibody (anti-chs7305 peptide antibody) 5′-TTT GAT ATC ATG TCC TCT CGT CAC GAC GAC was carried out in a 1:50 dilution overnight at 4 °C. After TC-3′ and 5′-ATA GGT ACC GCT CAT GCT ACG TTT thorough washing, anti-mouse IgG conjugated with Cru- GCT CCT CG-3′ (EcoRV and KpnI sites are underlined) zFluor488 (SantaCruz Biotechnology, Heidelberg, Ger- to achieve a fusion upstream to egfp (C-terminal fusion many) was applied in a 1:100 dilution. After incubation protein). Te PCR product was digested with EcoRV for 2 h at 23 °C, the sample was fnally washed with TBS and KpnI and ligated into the vector pTpNR/EcoRV/ and analyzed by epifuorescence microscopy. KpnI/egfp. Furthermore, the oligonucleotides 5′-TTT Immunofuorescently labeled cells were also stained GAT ATC ATG TCC TCT CGT CAC GAC GAC TC-3′, with other fuorescent dyes. Calcofuor white was used 5′-GCT TCT GCG TCT TTC TCG TCA GGG TAC to stain chitin in labeled cells. Tose were incubated CTT T-3′, 5′-TTT GCG GCC GCT TGG CTT CTT in a 0.01% solution (Tris–HCl, pH 8.8) for 10 min at TGT GGG GAT CTT C-3′ and 5′-AAA GCG GCC GCT room temperature after immunolocalization. PDMPO CAG CTC ATG CTA CGT TTG CTC-3′ (EcoRV, KpnI (2-(4-pyridyl)-5-((4-(2-dimethylaminoethyl-aminocarba- and NotI restriction sites are underlined) were used to moyl)methoxy)-phenyl)oxazole) was used to stain newly obtain DNA fragments that split chs7305. Te resulting formed frustules. Terefore, PDMPO was added to the fragments were ligated in the vector pTpNR/EcoRV/KpnI/ growing culture 12 h prior to immunolocalization at a egfp/NotI to insert egfp into chs7305 (the point of inser- concentration of 10 µM. tion locates in an extracellular domain of the correspond- Epifuorescence analysis was carried out with a LSM ing protein sequence). Te subsequent introduction of 780 laser scanning microscope (Zeiss, Göttingen, Ger- the expression vectors into T. pseudonana by particle many) equipped with a laser diode (405 nm), Ar laser bombardment and selection of recombinant cells on (488 nm) and HeNe laser (633 nm). Te detection of nourseothricin-containing agar plates was performed as fuorescence signals was achieved with a photomulti- described previously [21]. Successfully selected mutants plier with adjustable band width. Fluorescence images were further analyzed by fuorescence microscopy and were also recorded on an Axio Observer Z1 (Zeiss, Göt- Western blotting. tingen, Germany) equipped with a metal halide UV lamp Wustmann et al. BMC Mat (2020) 2:10 Page 3 of 7 and the flters FS 49: EX BP 347/55; BS LP 395; EM BP conducted with SuperSignal WestPico (TermoScientifc; 445/50 (Dapi) FS 38 HE: EX BP 470/40; BS LP 495; EM Rockford, USA) and detected on an Amersham X-Ray BP 525/50 (GFP) and FS 50 HE: EX BP 640/30; BS LP flm (GE Healthcare, Heidelberg, Germany).
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