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Nitrogen Deprivation-Induced Production of Volatile Organic fmars-07-00410 June 5, 2020 Time: 19:43 # 1 ORIGINAL RESEARCH published: 09 June 2020 doi: 10.3389/fmars.2020.00410 Nitrogen Deprivation-Induced Production of Volatile Organic Compounds in the Arachidonic-Acid-Accumulating Microalga Lobosphaera incisa Underpins Their Role as ROS Scavengers and Chemical Messengers Edited by: Yuji Hiwatashi, Puja Kumari†, Alon Cna’ani, Shoshana Didi-Cohen, Vered Tzin and Miyagi University, Japan Inna Khozin-Goldberg* Reviewed by: French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Susana Puntarulo, Ben-Gurion University of the Negev, Beersheba, Israel University of Buenos Aires, Argentina Tiziano Verri, University of Salento, Italy The green microalga Lobosphaera incisa accumulates long-chain polyunsaturated *Correspondence: arachidonic acid sequestered in triacylglycerols under nitrogen (N)-starvation conditions. Inna Khozin-Goldberg [email protected] Many of L. incisa’s physiological and metabolic responses to N-starvation have †Present address: been previously investigated. However, the temporal dynamics of the volatile organic Puja Kumari, compounds (VOCs) under different N availability and their role in L. incisa stress Faculty of Fisheries Sciences, responses have yet to be elucidated. Here, we investigated the VOC profiles of L. Hokkaido University, Hakodate, Japan incisa to reveal their emission patterns, and proposed their physiological roles under Specialty section: N-starvation. Using gas chromatography-mass spectrometry, 42 and 19 VOCs were This article was submitted to Aquatic Physiology, identified in the algal biomass (AVOCs) and in the medium (MVOCs), respectively, a section of the journal belonging to alkanes, alkenes, benzenoids, esters, fatty alcohols, fatty aldehydes, Frontiers in Marine Science fatty acids (FAs), FA esters, ketones, and terpenoids; most of these are the oxidative Received: 31 March 2020 products of FAs or photosynthetic pigment degradation. The discriminant AVOCs and Accepted: 12 May 2020 Published: 09 June 2020 MVOCs produced under N-starvation were identified by principal component analyses Citation: and hierarchical clustering. A significant treatment- and time-dependent increase in Kumari P, Cna’ani A, volatile FAs and their oxidative products was observed in the algal biomass and Didi-Cohen S, Tzin V and Khozin-Goldberg I (2020) Nitrogen medium under N-starvation as compared to N-replete controls, following a similar Deprivation-Induced Production pattern as reactive oxygen species (ROS) production. This suggests that VOCs may be of Volatile Organic Compounds involved in ROS scavenging. Despite the increase in total VOCs, terpenoids and alkenes in the Arachidonic-Acid-Accumulating Microalga Lobosphaera incisa decreased significantly with N-starvation duration, along with chloroplast degradation. Underpins Their Role as ROS Transcriptomics data supported the VOC patterns and revealed the upregulation Scavengers and Chemical Messengers. Front. Mar. Sci. 7:410. of genes involved in fatty aldehyde, fatty alcohol, and ketone synthesis, including doi: 10.3389/fmars.2020.00410 lipoxygenase, thioesterase, and fatty acyl CoA reductase, along with a decrease in Frontiers in Marine Science | www.frontiersin.org 1 June 2020 | Volume 7 | Article 410 fmars-07-00410 June 5, 2020 Time: 19:43 # 2 Kumari et al. Production of Volatiles Under Nitrogen-Starvation the expression of genes putatively implicated in alkene biosynthesis. Several VOCs were identified as potential biotechnological targets, and their putative biosynthetic pathways were proposed, which could be genetically manipulated to enhance the yields of high value products. We conclude that VOCs may play an important role in stress metabolism, ROS scavenging, and the amelioration of oxidative stress under N-starvation. Also, VOCs released in the medium may communicate the signal to neighboring cells, thus priming them to adjust their metabolic activities to adapt to N-starvation conditions, indicating that the function of VOCs as chemical signaling messengers is conserved from microalgae to higher plants. Keywords: Lobosphaera incisa, lipoxygenase, nitrogen stress, polyunsaturated aldehydes, reactive oxygen species, volatiles INTRODUCTION The emission of VOCs in microalgal cultures can vary across different species and is affected by environmental conditions. Microalgae constitute a diverse group of predominantly Both abiotic and biotic factors elicit VOC generation in photosynthetic and aquatic eukaryotic microorganisms, with microalgal cultures, such as temperature, light, nutrients, pH, high ecophysiological and biotechnological significance. salinity, oxidative stress, wounding, and predators (Achyuthan Microalgae, particularly planktonic species, are known to et al., 2017). Furthermore, the VOC emission spectra may produce a variety of volatile organic compounds (VOCs) be species- and condition-specific, hence serving as useful with important roles in ecology, atmospheric chemistry, biomarkers of culture stage, health, performance, and the and global climate. VOCs comprise low molecular weight presence of predators. In addition, VOCs hold promise as compounds with low to moderate hydrophilicity and high-value by-products with a range of applications in the ◦ high vapor pressure at ambient conditions (20 C and food and biofuels industry (Achyuthan et al., 2017). VOCs are 101.3 kPa). The dispersal of VOCs at the air-water interface considered to be the main by-products formed during growth facilitates their infochemical effects on both terrestrial under phototrophic conditions and may represent up to 90% and aquatic organisms. Infochemicals are chemical cues of the total carbon substrate converted in the photobioreactor, emitted or secreted by organisms that influence ecological as indicated by a carbon balance analysis (Jacob-Lopes and interactions in nature. The VOC metabolic profile of an Franco, 2013). Understanding the mechanisms underlying VOC organism has been termed “volatilome” (or “volatome”), emission and characterizing the volatile fraction can establish and the respective field of study is called volatilomics routes for the bioconversion of desired substrates, enabling (Achyuthan et al., 2017). potential applications of the volatile molecules (Jacob-Lopes Studies on the volatilomes of cultivated microalgal species is et al., 2010; Jacob-Lopes and Franco, 2013). Despite diversity still in its infancy. VOCs produced by microalgae are known and importance of microalgal VOCs, little quantitative or genetic to include volatile aldehydes, alcohols, esters, carboxylic acids, information is available on VOC biogeneration in vivo or on hydrocarbons, ketones, furans, fatty acids derived from lipid their biochemistry and environmental impact, in particular by metabolic pathways, carotenoid and terpene derivatives (ionones, green microalgae (Chlorophyta), as compared to higher plants, cyclocitrals), sulfur, and halogenated compounds (Santos et al., phytoplankton, and macroalgae. 2016; Achyuthan et al., 2017; Zhou et al., 2017; Hosoglu, 2018). Plant volatiles (especially C6 aldehydes and alcohols, called green leaf volatiles) are involved in plant-herbivore Abbreviations: ALA, a-linolenic acid; ANOVA, One-way analysis of tritrophic and intraspecific interactions. They also play a role variance; ARA, arachidonic acid; AVOCs, VOCs identified in algal biomass; in pollination, and communications within and between plant Car, carotenoids; CER 1, eceriferum 1; Chl, chlorophyll; DCF- 20,70, dichlorofluorescein; DCF-FU, 20;70-dichlorofluorescein fluorescent unit; communities (Kihara et al., 2014; Ameye et al., 2018). In marine DCFH-DA, dichlorodihydrofluorescein diacetate; DW, dry weight; FA, fatty systems, macroalgae-derived volatiles, mainly represented by acid; FAME, fatty acid methyl esters; FAP, fatty acid photodecarboxylase; organic halogens, aldehydes, and dimethyl sulfide, are involved FAR, fatty acyl (CoA) ACP reductase; FID, flame ionization detector; GC-MS, in defense and trophic interactions (Jerkovic´ et al., 2018; gas chromatography mass spectrometry; GMC, glucose-methanol-choline oxidoreductase; HPETE, hydroperoxyeicosatetraenoic acid; HPL, hydroperoxide Song et al., 2018; Zhu et al., 2018). Phytoplankton-derived lyase; HPOT, hydroperoxyoctadecadienoic acid; IBB, Isobutylbenzene; KAR, 3- VOCs are known for the eco-physiological roles they play ketoacyl-ACP reductase; LA, linoleic acid; LACS, long-chain acyl-CoA synthetase; in the aquatic environment, acting as info(semio)chemicals LOX, lipoxygenase; MUFAs, monounsaturated fatty acids; MVOCs, VOCs identified in culture medium; OA, oleic acid; PCA, principal component analysis; in intraspecific (pheromones) and interspecific (kairomones) PES, phytyl ester synthase; PGD1, plastid galactoglycerolipid degradation1; communication, predator-prey interactions, activated defenses, PUFA, polyunsaturated fatty acid; ROS, reactive oxygen species; SFAs, saturated interspecific non-communicative interactions, mainly fatty acids; SPME, solid-phase microextraction; TAG, triacylglycerol; TFA, total involving dimethyl sulfide, dimethylsulfoniopropionate and fatty acid; TVOCs, total volatile organic compound; VOCs, volatile organic compounds; Vol, volumetric. short-chain polyunsaturated aldehydes (PUAs), and their Frontiers in Marine Science | www.frontiersin.org 2 June 2020 | Volume 7 | Article 410 fmars-07-00410 June 5, 2020 Time: 19:43 # 3 Kumari et al. Production of Volatiles Under Nitrogen-Starvation enhancing of
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