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      Ectoine from Bacterial and Algal Origin Is a Compatible Solute in Microalgae

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          Abstract

          Osmoregulation in phytoplankton is attributed to several highly polar low-molecular-weight metabolites. A widely accepted model considers dimethylsulfoniopropionate (DMSP) as the most important and abundant osmotically active metabolite. Using an optimized procedure for the extraction and detection of highly polar metabolites, we expand the group of phytoplankton osmolytes by identifying ectoine in several microalgae. Ectoine is known as a bacterial compatible solute, but, to the best of our knowledge, was never considered as a phytoplankton-derived product. Given the ability of microalgae to take up zwitterions, such as DMSP, we tested the hypothesis that the algal ectoine is derived from associated bacteria. We therefore analyzed methanol extracts of xenic and axenic cultures of two different species of microalgae and could detect elevated concentrations of ectoine in those that harbor associated bacteria. However, also microalgae without an associated microbiome contain ectoine in smaller amounts, pointing towards a dual origin of this metabolite in the algae from their own biosynthesis as well as from uptake. We also tested the role of ectoine in the osmoadaptation of microalgae. In the model diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum, elevated amounts of ectoine were found when cultivated in seawater with salinities of 50 PSU compared to the standard culture conditions of 35 PSU. Therefore, we add ectoine to the family of osmoadaptive metabolites in phytoplankton and prove a new, potentially synergistic metabolic interplay of bacteria and algae.

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          Most cited references38

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          New and important roles for DMSP in marine microbial communities

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            Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells.

            In order to get the high liquefaction yield from marine algae cell mass to fuel oil, the effect of salt stress on the accumulation of lipids and triacylglyceride in Dunaliella cells was investigated. Although initial NaCl concentration higher than 1.5 M markedly inhibited cell growth, increase of initial NaCl concentration from 0.5 (equal to sea water) to 1.0 M resulted in a higher intracellular lipid content (67%) in comparison with 60% for the salt concentration of 0.5 M. Addition of 0.5 or 1.0 M NaCl at mid-log phase or the end of log phase during cultivation with initial NaCl concentration of 1.0 M further increased the lipid content (70%).
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              Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes.

              The compatible solute dimethylsulphoniopropionate (DMSP) has important roles in marine environments. It is an anti-stress compound made by many single-celled plankton, some seaweeds and a few land plants that live by the shore. Furthermore, in the oceans it is a major source of carbon and sulphur for marine bacteria that break it down to products such as dimethyl sulphide, which are important in their own right and have wide-ranging effects, from altering animal behaviour to seeding cloud formation. In this Review, we describe how recent genetic and genomic work on the ways in which several different bacteria, and some fungi, catabolize DMSP has provided new and surprising insights into the mechanisms, regulation and possible evolution of DMSP catabolism in microorganisms.
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                Author and article information

                Journal
                Mar Drugs
                Mar Drugs
                marinedrugs
                Marine Drugs
                MDPI
                1660-3397
                06 January 2020
                January 2020
                : 18
                : 1
                : 42
                Affiliations
                [1 ]Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich Schiller University, Lessingstrasse 8, D-07743 Jena, Germany; simona.fenizia@ 123456uni-jena.de (S.F.); Kathleen.thume@ 123456uni-jena.de (K.T.); Marino.wirgenings@ 123456uni-jena.de (M.W.)
                [2 ]Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, D-07745 Jena, Germany
                Author notes
                Author information
                https://orcid.org/0000-0003-2351-6336
                Article
                marinedrugs-18-00042
                10.3390/md18010042
                7024275
                31935955
                d6bba373-006a-4476-a289-140becc6711f
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 17 November 2019
                : 23 December 2019
                Categories
                Article

                Pharmacology & Pharmaceutical medicine
                ectoine,osmoadaptation,compatible solutes,phytoplankton,lc/ms analysis,osmoregulation,diatoms,dmsp

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