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. 2018 Jul;169(3):406-431.
doi: 10.1016/j.protis.2018.03.002. Epub 2018 Mar 20.

New Taxa of Streptophyte Algae (Streptophyta) from Terrestrial Habitats Revealed Using an Integrative Approach

Tatiana Mikhailyuk  1 , Alena Lukešová  2 , Karin Glaser  3 , Andreas Holzinger  4 , Sabrina Obwegeser  4 , Svetlana Nyporko  5 , Thomas Friedl  6 , Ulf Karsten  3
Affiliations

New Taxa of Streptophyte Algae (Streptophyta) from Terrestrial Habitats Revealed Using an Integrative Approach

Tatiana Mikhailyuk et al. Protist. 2018 Jul.

Abstract

Two new genera (Streptosarcina and Streptofilum) and three new species (Streptosarcina arenaria, S. costaricana and Streptofilum capillatum) of streptophyte algae were detected in cultures isolated from terrestrial habitats of Europe and Central America and described using an integrative approach. Additionally, a strain isolated from soil in North America was identified as Hormidiella parvula and proposed as an epitype of this species. The molecular phylogeny based on 18S rRNA and rbcL genes, secondary structure of ITS-2, as well as the morphology of vegetative and reproductive stages, cell ultrastructure, ecology and distribution of the investigated strains were assessed. The new genus Streptosarcina forms a sister lineage to the genus Hormidiella (Klebsormidiophyceae). Streptosarcina is characterized by packet-like (sarcinoid) and filamentous thalli with true branching and a cell organization typical for Klebsormidiophyceae. Streptofilum forms a separate lineage within Streptophyta. This genus represents an easily disintegrating filamentous alga which exhibits a cell coverage of unique structure: layers of submicroscopic scales of piliform shape covering the plasmalemma and exfoliate inside the mucilage envelope surrounding cells. The implications of the discovery of the new taxa for understanding evolutionary tendencies in the Streptophyta, a group of great evolutionary interest, are discussed.

Keywords: Hormidiella; Streptofilum; Streptophyta; Streptosarcina; integrative approach; ultrastructure..

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Figures

Fig. 1
Fig. 1
Molecular phylogeny of Streptophyta based on concatenated dataset 18S rRNA and rbcL sequences. Phylogenetic tree was inferred by Bayesian method with Bayesian Posterior Probabilities (PP) and maximum likelihood (ML) bootstrap support (BP) indicated at nodes. From left to right, support values correspond to ML BP and Bayesian PP; BP values lower than 50% and PP lower than 0.8 not shown. Strains marked with bold are newly sequenced isolates. Clade designations follow Leliaert et al. (2012).
Fig. 2
Fig. 2
Comparison of ITS-2 secondary structure of Hormidiella strains. The structure of H. parvula (Luk-89) is presented with the differences to H. attenuata (CCAP 329/1) highlighted. Variable bases or base pairs of H. attenuata are shown with circles.
Fig. 3
Fig. 3
Comparison of ITS-2 secondary structure of Streptosarcina strains. The structure of S. arenaria (AL-63) is presented with the differences to another strain of S. arenaria (Prim 3-3) and to S. costaricana (SAG 36.98). Variable bases or base pairs of S. arenaria (Prim 3-3) are shown with boxes and S. costaricana (SAG 36.98) with circles.
Fig. 4
Fig. 4
Morphology and reproduction of Hormidiella parvula (Luk-89). A–C) Vegetative filaments in adult (A, B) and young state (C). D) Formation of sporangia (arrows). E) Empty sporangia with openings in cell wall (arrows). F) Zoospore. G) Stopped zoospore, formation of papilla (arrow). H, I) Germination of young filament with the stalk. J) H-like fragments of cell wall (arrows). Scale bars: A–E, J are 10 μm, F–I are 5 μm.
Fig. 5
Fig. 5
Morphology and reproduction of Streptosarcina gen. nov. A–G) S. arenaria sp. nov. (AL-63 (B, C) and Prim-3-3 (A, D-G). A, B, D). Packet-like vegetative thallus. C) Filaments. E, F) Formation of sporangia (arrows) and empty sporangia with openings in cell wall (arrowheads). G) Stopped zoospores. H–M) S. costaricana sp. nov. (SAG 36.98). H) Unicellular stage, nucleus (arrowhead) and terminal vacuoles (arrows) are visible. I-K) Branching of filaments. L, M) Elongated cells with multiple pyrenoids from old culture, H-like fragments of cell wall are visible (arrows). Scale bars are 10 μm.
Fig. 6
Fig. 6
Morphology of Streptofilum capillatum gen. et sp. nov. (Luk-316a). A–C) Filaments and cell dyads surrounded by mucilage envelope (arrows). D–H) Mucilage staining by methylene blue. Homogenous mucilage envelope with lobbed edge (arrows) and collar structures (arrowheads) are visible. Scale bars: A–E are 10 μm, F–H are 5 μm.
Fig. 7
Fig. 7
Drawings of Hormidiella, Streptosarcina and Streptofilum species. A–E) Morphology and reproduction of Hormidiella parvula A) Vegetative filament. B) Sporangia (arrows) and empty sporangia with openings in cell wall (arrowheads). C) Zoospore. D) Stopped zoospore, formation of papilla (arrow). E) Germination of young filament with the stalk. F–H) Streptosarcina arenaria sp. nov. F) Packet-like vegetative thallus. G). Sporangium (arrow) and empty sporangium with opening in cell wall (arrowhead). H) Zoospore and stopped zoospore. I–K) S. costaricana sp. nov. I) Unicellular stage, nuclei (arrowheads) and terminal vacuoles (arrows) are visible. J) Elongated cell with multiple pyrenoids from old culture, H-like fragments of cell wall are visible (arrows). K) Branching of filaments. L–N) Morphology and ultrastructure of Streptofilum capillatum gen. et sp. nov. L) Filament and cell dyad surrounded by mucilage envelope, nuclei (arrowheads) are visible. M, N) Reconstruction of TEM micrographs with details of cell ultrastructure and coverage. Scale bars: A–L are 10 μm, M, N is 5 μm.
Fig. 8
Fig. 8
Transmission electron micrographs of Hormidiella and Streptosarcina species. A, B) H. parvula (Luk-89). A) Cell in overview. B) Portion of cell showing closely arranged chloroplast, peroxisome and nucleus. C-F) S. arenaria gen. et sp. nov. (Prim-3-3). C) Cell in overview. D–F) Portions of cells showing closely arranged chloroplast, peroxisome and nucleus, pyrenoid traversable by parallel thylakoids, centrioles and chloroplast structure. G–I) S. costaricana gen. et sp. nov. (SAG 36.98). G) Cell in overview. H, I) Portions of cells showing closely arranged chloroplast, peroxisome and nucleus, pyrenoid traversed by parallel arranged thylakoids and chloroplast structure. Abbreviations: Ch, chloroplast; Py, pyrenoid; S, starch; N, nucleus, Nu, nucleolus; P, peroxisome; M, mitochondrium, G, Golgi body; C, centrioles; CW, cell wall. Scale bars: A–E, G–I are 1 μm, F is 0.5 μm.
Fig. 9
Fig. 9
Transmission electron micrographs of Streptofilum capillatum gen. et sp. nov. (Luk-316a). A) Cell in overview showing pyrenoid, chloroplast and cell coverage by scales. B) Portion of cell showing closely arranged chloroplast, peroxisome and nucleus. C-E) Cell coverage forming by scales in section (C, D) and surface section (E). F, G) Origination of scales inside cells (likely transported to cell surface). Abbreviations: Ch, chloroplast; Py, pyrenoid; S, starch; N, nucleus; Nu, nucleolus; P, peroxisome; M, mitochondria; L, lipid globules; CC, cell coverage; Mu, mucilage, Sc, scales in the inner parts of the cell, likely prior to deposition to the cell surface. Scale bars: A, E are 1 μm, B-D, F, G are 0.5 μm.
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