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

Simona Fenizia,Marino Wirgenings,Kathleen Thume,Georg Pohnert

doi:10.3390/md18010042

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.

Highlights

Diatoms are photosynthetic unicellular algae, responsible for 20% of global carbon fixation and 40% of marine primary production
To identify novel zwitterionic metabolites involved in the osmoadaptation of marine organisms, we analyzed the endometabolome of the diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum using ultra-high-pressure liquid chromatography high-resolution mass spectrometry (UHPLC–HRMS)
Algae were grown at standard culture conditions of 35 Practical Salinity Units (PSU, g NaCl kg−1 sea water) and under increased salinity of 50 PSU, where the growth of T. weissflogii still follows a standard growth curve with slightly reduced cell counts [14]

Summary

Introduction

Diatoms are photosynthetic unicellular algae, responsible for 20% of global carbon fixation and 40% of marine primary production They are important producers of zwitterionic metabolites, a class of small organic compounds that has central osmoregulatory, antioxidant, and cryoprotectant functions [1,2]. Other sulfur-containing metabolites, like dimethylsulfonioacetate (DMSA), gonyol, and the most recently identified dimethylsulfoxonium propionate (DMSOP); as well as nitrogen-containing metabolites, like glycine betaine (GBT), homarine, and trigonelline, have been discovered and studied in phytoplankton as well [2,4] These metabolites are classified as “compatible solutes”, organic water-soluble compounds accumulated by micro-organisms either by de novo synthesis or by uptake

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