Early Embryogenesis of Brown Alga Fucus Vesiculosus L. Is Characterized by Signiﬁcant Changes in Carbon and Energy Metabolism

molecules Article Early Embryogenesis of Brown Alga Fucus vesiculosus L. is Characterized by Significant Changes in Carbon and Energy Metabolism Elena Tarakhovskaya 1,*,†, Valeriya Lemesheva 1, Tatiana Bilova 1 and Claudia Birkemeyer 2,† ID 1 Department of Plant Physiology and Biochemistry, Faculty of Biology, St.-Petersburg State University, 199034 St.-Petersburg, Russia; [email protected] (V.L.); [email protected] (T.B.) 2 Faculty of Chemistry and Mineralogy, Leipzig University, 04103 Leipzig, Germany; [email protected] * Correspondence: [email protected]; Tel.: +7-911-918-2745 † These authors contributed equally to this work. Received: 21 August 2017; Accepted: 8 September 2017; Published: 9 September 2017 Abstract: Brown algae have an important role in marine environments. With respect to their broad distribution and importance for the environment and human use, brown algae of the order Fucales in particular became a model system for physiological and ecological studies. Thus, several fucoids have been extensively studied for their composition on the molecular level. However, research of fucoid physiology and biochemistry so far mostly focused on the adult algae, so a holistic view on the development of these organisms, including the crucial first life stages, is still missing. Therefore, we employed non-targeted metabolite profiling by gas chromatography coupled to mass spectrometry to create a non-biased picture of the early development of the fucoid alga Fucus vesiculosus. We found that embryogenic physiology was mainly dominated by a tight regulation of carbon and energy metabolism. The first dramatic changes of zygote metabolism started within 1 h after fertilization, while metabolism of 6–9 days old embryos appeared already close to that of an adult alga, indicated by the intensive production of secondary metabolites and accumulation of mannitol and citric acid. Given the comprehensive description and analysis we obtained in our experiments, our results exhibit an invaluable resource for the design of further experiments related to physiology of early algal development. Keywords: Fucus; metabolomics; GC-MS; embryogenesis; zygote; brown algae 1. Introduction Brown algae of the order Fucales inhabit the intertidal zone of rocky seashores almost throughout the world, with the bladderwrack, Fucus vesiculosus, as one of the most common species. Fucoids have a broad use for humans, for instance in food, cosmetic skin treatment, industry (including algal biomass production for biofuels), phytoremediation, or as metal content bioindicators [1–5]. Moreover, metabolic substrates of these algae are currently extensively explored in medical research, for example related to their action upon cancer cells, their pro- and anticoagulant effects and others [6]. These multiple uses highlight the importance these organisms have to humans and explain the interest scientists all over the world develop for the physiological aspects in fucoid development. Thus, fucoid embryogenesis became a generally applied model system used to study numerous aspects of algal physiology, including cell polarization, cell wall assembly, photosynthetic performance, and bioadhesion (e.g., [7–11]). The principal feature of this process making it so attractive to investigate is that fucoid zygotes and embryos develop independently of maternal tissues which makes them easily accessible for experimental studies at all developmental stages. The gametes of these algae are released Molecules 2017, 22, 1509; doi:10.3390/molecules22091509 www.mdpi.com/journal/molecules Molecules 2017, 22, 1509 2 of 16 Molecules 2017, 22, 1509 2 of 17 fromgametes conceptacles of these into algae the are water, released where from eggs conceptacles are fertilized into and the zygoteswater, where germinate. eggs are Fucoid fertilized eggs and have a sphericalzygotes shape, germinate. they Fucoid are initially eggs have apolar a spherical and have shap no celle, they wall are (Figure initially1). apolar The first and morphological have no cell wall sign of development(Figure 1). The can first be observedmorphological within sign ca. of 14–16 development h after fertilization can be observed (AF), when within a rhizoid ca. 14–16 protuberance h after appearsfertilization on the (AF), zygote when surface a rhizoid according protuberance to the developed appears on polarity the zygote axis [surface12,13]. Theaccording polarization to the of fucoiddeveloped zygotes polarity has been axis extensively [12,13]. The investigated polarization (e.g.,of fucoid [10,14 zygotes,15]). Thehas been rhizoid extensively appearance investigated is preceded by(e.g., a series [10,14,15]). of complicated The rhizoid physiological appearance processes, is preceded including by asymmetrica series of complicated ion fluxes [10 physiological], redistribution of cytoskeletalprocesses, including elements asymmetric [16], and targetedion fluxes vesicular [10], redistribution secretion [ 15of]. cytoskeletal The next critical elements morphological [16], and eventtargeted is the vesicular first division secretion of the [15]. zygote, The which next critical is asymmetrical morphological and proceeds event is inthe the first plane division perpendicular of the to thezygote, formed which polarity is asymmetrical axis. Daughter and proceeds cells differ in the distinctly plane perpendicular in structure to and the fate:formed one polarity of them axis. gives riseDaughter to the thallus cells differ of the distinctly alga and in the structure other to and rhizoid fate: one [12, 17of ].them The gives rhizoid rise cell to the elongates thallus rapidlyof the alga by tip growth,and the dividing other transverselyto rhizoid [12,17]. to the The growth rhizoid axis andcell creatingelongates a rapidly file of cells. by tip During growth, next dividing three days (2–4transversely days AF), theto the rhizoid growth remains axis and the creating only site a file of conspicuousof cells. During growth next three in the days embryo. (2–4 days The AF), thallus the cell rhizoid remains the only site of conspicuous growth in the embryo. The thallus cell undergoes a series undergoes a series of proliferative divisions, each division being transverse to the previous one, that of proliferative divisions, each division being transverse to the previous one, that gives rise to an gives rise to an elongated multicellular structure—the thallus part of the embryo [13,17]. In 7–8 days elongated multicellular structure—the thallus part of the embryo [13,17]. In 7–8 days AF, several AF, several inner cells of the thallus part start producing specific filamentous structures—the apical inner cells of the thallus part start producing specific filamentous structures—the apical hairs. Apical hairs.hair Apicalinitiation hair is a initiation crucial stage is a in crucial fucoid stageembryo ingenesis, fucoid because embryogenesis, subsequently because the basal subsequently cell of one the basalof these cell of hairs one becomes of these hairsthe apical becomes meristematic the apical cell meristematic of the future cell plant, of the giving future rise plant, to the giving apical rise to themeristem apical of meristem adult alga of [18,19]. adult Simultaneously alga [18,19]. Simultaneously or soon after this or first soon sign after of starting this first organogenesis, sign of starting organogenesis,the primary rhizoid the primary generates rhizoid branches generates forming branches a stipe-like forming structure a stipe-like which structure allow the which embryo allow to the embryoattach tobetter attach to the better substratum. to the substratum. From this moment, From this the moment, basic body the plan basic of future body planalga is of established, future alga is established,so that early so embryogenesis that early embryogenesis is finished after is finished 9 days after after fertilization. 9 days after fertilization. FigureFigure 1. 1.Scheme Scheme of ofF. F. vesiculosus vesiculosusearly early embryogenesis.embryogenesis. AFAF—after—after fertilization; fertilization; az—antherozoids;az—antherozoids; cwcw—cell—cell wall; wall;adh adh—adhesive—adhesive material; material;ves ves—secretory—secretory vesicles. Fucoids are oogamic plants, and their eggs have a reserve of storage compounds such as mannitolFucoids and are oogamiclaminaran. plants, Noteworthy, and their eggsfucoid have eggs a reservealready of can storage carry compounds out photosynthesis, such as mannitol the andefficiency laminaran. of which Noteworthy, grows rapidly fucoid du eggsring already the first can days carry after out fertilizat photosynthesis,ion [20]. The the schedule efficiency of fucoid of which growsembryogenesis rapidly during is very the tight—cell first days wall after formation fertilization starts [ 20minutes]. The after schedule fertilization, of fucoid between embryogenesis 3 and 6 h is veryAF tight—cell zygotes attach wall themselves formation to starts the substrate minutes afterand become fertilization, sensitive between to the polarizing 3 and 6 h AFcues, zygotes until 12 attach h themselvesAF the polarity to the axis substrate should and be fixed become etc. [9,15] sensitive. Besides to the the polarizing basic processes cues, maintaining until 12 h AF growth the polarity and axisdevelopment, should be fixed the etc.establishment [9,15]. Besides of the the elabor basicate processes mechanisms maintaining of the growthcell responses and development, to the theenvironmental establishment factors of the elaboratealso takes mechanismsplace

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