Unicellular versus Filamentous: The Glacial Alga Ancylonema alaskana comb. et stat. nov. and Its Ecophysiological Relatedness to Ancylonema nordenskioeldii (Zygnematophyceae, Streptophyta)

Abstract

Melting polar and alpine ice surfaces frequently exhibit blooms of dark pigmented algae. These microbial extremophiles significantly reduce the surface albedo of glaciers, thus accelerating melt rates. However, the ecology, physiology and taxonomy of cryoflora are not yet fully understood. Here, a Swiss and an Austrian glacier dominated either by filamentous Ancylonema nordenskioeldii or unicellular Mesotaenium berggrenii var. alaskanum, were sampled. Molecular analysis showed that both species are closely related, sharing identical chloroplast morphologies (parietal-lobed for Ancylonema vs. axial plate-like for Mesotaenium sensu stricto), thus the unicellular species was renamed Ancylonema alaskana. Moreover, an ecophysiological comparison of the two species was performed: pulse-amplitude modulated (PAM) fluorometry confirmed that they have a high tolerance to elevated solar irradiation, the physiological light preferences reflected the conditions in the original habitat; nonetheless, A. nordenskioeldii was adapted to higher irradiances while the photosystems of A. alaskana were able to use efficiently low irradiances. Additionally, the main vacuolar polyphenol, which effectively shields the photosystems, was identical in both species. Also, about half of the cellular fatty acids were polyunsaturated, and the lipidome profiles dominated by triacylglycerols were very similar. The results indicate that A. alaskana is physiologically very similar and closely related but genetically distinct to A. nordenskioeldii.

Keywords: Mesotaeniaceae; cryoflora; fatty acids; lipidome; photosynthesis; phylogeny; polyphenols; supraglacial communities.

Figure 1

Light microphotographs of cells collected from melting glacier surfaces in the European Alps, (a–d) Ancylonema alaskana comb. et stat. nov. (WP167) and (e,f) Ancylonema nordenskioeldii (WP211). (a) transient stage of two cells after cleavage (upper right), showing one parietal chloroplast per cell in the side view (upper right and middle) or two chloroplasts before cell cleavage (lower left) (WP167), (c) elongated cell with two chloroplasts, (a–d) corresponding bright field and fluorescence images, the latter reveal the partly lobed chloroplast shape. (e) side view demonstrating two parietal chloroplasts per cell (or one with two pyrenoids), (f) group of dark pigmented filaments, most of them with 2, 4 or 8 cells, but also single individuals were present (arrowheads). Scale: 10 μm.

Figure 2

18S rRNA gene-based maximum-likelihood phylogenetic tree of the Zygnematophyceae. The ‘Ancylonema’-clade is highlighted (grey box). All the other labelled clades correspond to [21]. Posterior probabilities (≥0.95) and bootstrap values from maximum likelihood analyses (≥50%) are shown. Full statistical support (1.00/100) is marked with an asterisk. Thick branches represent nodes receiving the highest posterior probability support (1.00). Newly obtained sequence is in bold. Accession numbers, strain or field sample codes are indicated after each species name.

Figure 3

The rbcL gene-based maximum-likelihood phylogenetic tree of selected Zygnematales. The names of clades correspond to [21]. Posterior probabilities (≥0.95) and bootstrap values from maximum likelihood analyses (≥50%) are shown. Full statistical support (1.00/100) is marked with an asterisk. Thick branches represent nodes receiving the highest posterior probability support (1.00). Newly obtained sequence in bold. Accession numbers, strain or field sample codes are indicated after each species name.

Figure 4

Photosynthetic rapid light curves of Ancylonema alaskana (pink circles) and Ancylonema nordenskioeldii (blue triangles). The effect of increasing photon fluence rates (x-axis) on the relative electron transport rate (rETR; y-axis) in chloroplasts was measured with field samples (WP167 and WP211) (n = 4, ±SD). The maximal rETR value achieved at 1500 µmol photons m⁻² s⁻¹ (*). The data points were fitted to the model, assuming no photoinhibition [39].

Figure 5

Cellular lipid composition of Ancylonema nordenskioeldii (WP211) and Ancylonema alaskana (WP167). (a) The relative proportions of lipid classes in (%) of total lipids. (b) The relative abundance of the most abundant lipid representatives of triacylglycerols (TAGs), sphingolipids (GIPCs, GlcCers), glycolipids (MGDG, SQDG), phospholipids (PG, PC),diacylglycerols (DAGs). The figure (b) shows only lipids that had abundances greater than 7% in a relevant lipid class.

Figure 6

Cellular fatty acid composition Ancylonema nordenskioeldii (blue; WP211) and Ancylonema alaskana (pink; WP251). (a) The relative proportions of fatty acids in (%) of total fatty acids. (b) The relative proportion of saturated (SAFA), monounsaturated (MUFA), and polyunsaturated (PUFA) fatty acids. The figure (a) shows only fatty acids that had abundances greater than 0.1% of total FAs.