The red alga Tsunamia transpacifica (Stylonematophyceae) from plastic drift shows adaptation to its uncommon habitat in ultrastructure and soluble low molecular weight carbohydrate composition

Andreas Holzinger,Christopher D Goodman,Christina Oppermann,Ancuela Andosch,Wolfgang Ruth,Sabrina Obwegeser,Ursula Lütz-Meindl,John A West,Ulf Karsten,Allison Van De Meene

doi:10.1007/s00709-021-01674-6

Abstract

The recently described red alga Tsunamia transpacifica (Stylonematophyceae) was previously isolated from plastic drift found at the pacific coast, but the natural habitat remains unknown. Here, we investigate ultrastructural details and the low molecular weight soluble carbohydrate composition to get further insight into the adaptation to this uncommon habitat. By means of high pressure freeze fixation, followed by freeze substitution, we could detect an up to 2-µm-thick cell wall surrounded by a distinct layer of extracellular polymeric substances (EPS), likely responsible for the adhering capacities of Tsunamia. The central position of the nucleus and multilobed parietal chloroplast, already observed by light microscopy, could be confirmed. The ultrastructure revealed large electron-dense bodies (EB) in the central cytoplasm, likely resembling degradation products of the chloroplast. Interestingly, these structures contained phosphorous and cobalt, and iron was found in smaller rounded electron-dense bodies by electron energy loss spectroscopy (EELS). Accumulation of these elements suggests a high biosorption activity of Tsunamia. Liquid chromatography-mass spectrometry (LC–MS) data showed the presence of two heterosides (floridoside and digeneaside) together with the polyol sorbitol, which are known as organic osmolytes and compatible solutes. Taken together, these are the first observations on ultrastructural details, element storage and accumulation of protective compounds are contributing to our understanding of the ultrastructural and osmotic solute basis for the ability of Tsunamia to thrive on plastic surfaces.

Highlights

Tsunamia transpacifica cells had the typical appearance of a well-developed crust with horizontal and vertical branching (Fig. 1a)
We provide here ultrastructural evidence that in T. transpacifica, several cells covered by distinct cell walls are embedded together in an extracellular matrix composed of extracellular polymeric substances (EPS), which appears denser towards the outside
Our hypothesis on storage and protection mechanisms could be confirmed with the presented data

Summary

Introduction

The red alga Tsunamia transpacifica J.A. West, G.I. Hansen, G.C. Zuccarello et T. Hanyuda (West et al 2016), was previously detected on a rather uncommon. Habitat—plastic debris originating from a tsunami resulting from a tremendous earthquake off the pacific coast of Tohoku, Japan, that took place on March 11, 2011. The debris crossed the Pacific Ocean and started to emerge on the Northeastern Pacific shores since 2012, where a conspicuous pink colored red algal crust was isolated in 2015 (West et al 2016). Many so far unanswered questions came up; how this organism lives remains undetected in its natural habitat and what kind of structural and physiological properties would enable to survive in the changing habitat

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