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Vannella primoblina n. sp. – an unusual species of the genus Vannella (Amoebozoa, Discosea, Vannellida) with pronounced dorsal ridges and folds

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Abstract

Amoebae of the order Vannellida (Amoebozoa, Discosea) have a fairly recognizable spatulate, fan-shaped or semi-circular outlines and a wide area of frontal hyaloplasm. They can be easily distinguished from the other groups of lobose amoebae even by light microscopy. The dorsal side of these amoebae is usually smooth and rarely bears ridges or folds, which are never numerous or regular. We have isolated an unusual species of vannellid amoebae, called Vannella primoblina n. sp. from a terrestrial substrate. It has well-developed dorsal relief consisting of regularly appearing folds and ridges. This amoeba superficially resembles members of the genus Thecamoeba. However, molecular analysis showed that this strain belongs to the genus Vannella. This finding indicates that dorsal folds may also be a characteristic of some species of vannellid amoebae and probably are a functional detail of the cell morphology rather than an apomorphy of Thecamoebida lineage. Overall outlines of the cell and the presence of the expanded frontal hyaline area remains the most reliable characters used to differentiate vannellid amoebae from other gymnamoebae lineages.

Introduction

Lobose amoebae of the genus Vannella Bovee, 1965 (Amoebozoa, Discosea, Vannellida) are widespread in nature and were found in freshwater and marine habitats, as well as in hypersaline ponds and the soil (Bovee 1965, 1970; Bovee and Sawyer 1979; Kudryavtsev et al. 2019; Maciver et al. 2017; Page 1974, 1983, Page, 1988; Smirnov 2001; Smirnov et al. 2007, 2016; Smirnov and Fenchel 1996). In locomotion, these amoebae are flattened, fan-shaped, semicircular, crescent-shaped or spatulate. The cells move as a whole and never form discrete pseudopodia. A wide frontal area of ​​the hyaloplasm is usually noticeably thinner than the main body of the cell and occupies the frontal part of the moving cell. The hyaloplasm may extend to the lateral sides of the cell, forming a wide anterolateral hyaline crescent. The dorsal surface of the cell is usually smooth. Some species may have small thickenings in the hyaline area, similar to dorsal waves, but never form any kind of subpseudopodia. Few species show temporary longitudinal folds on the dorsal surface of the cell. These folds start in the hyaline area and last into the granuloplasm area of the cell (Page 1988, Page and Siemensma 1991; Smirnov and Brown 2004).

The genus Vannella was established by Bovee (1965), along with an update on the diagnosis of the genus Flabellula within the family Flabellulidae. The new group included amoebae with fan-shaped outlines in fast movement and wide shovel-like outlines during slow movement. A complex taxonomic history of the family Vannellidae was described in details by Smirnov et al. (2007). Currently, the genus Vannella Bovee, 1965 belongs to the family Vannellidae, subclass Flabellinia, class Discosea and is one of the most species-rich genera of lobose amoeba (Smirnov et al. 2007, 2011).

The first molecular data on vannellid amoebae settled this genus within the present class Discosea (Amaral-Zettler et al. 2006; Bolivar et al., 2001; Fahrni et al. 2003; Sims et al., 1999; Smirnov et al. 2002). Peglar et al. (2003) sequenced representatives of the genera Clydonella and Lingulamoeba established by Sawyer (1975a, 1975b) and showed that these genera represents an independent lineage related to the genus Vannella. Further studies indicated that species of the former genera Vannella and Platyamoeba are intermingled in the phylogenetic tree, while a species “Platyamoeba stenopodia” belongs to the family Thecamoebidae (Smirnov et al. 2007). Thus the genus Platyamoeba was merged with the genus Vannella, while Platyamoeba stenopodia was transferred to the family Thecamoebidae under the name Stenamoeba stenopodia (Smirnov et al. 2007) . The same study shows that the species Vannella platypodia has evident peculiarities in the SSU gene sequence, which is significantly shortened as compared to other vannellids. Based on this as well as on some morphological details, this species was transferred to the genus Ripella, which was further enriched with two more species (Kudryavtsev and Gladkikh 2017; Smirnov et al. 2007). Kudryavtsev (2014) described the genus Paravannella, which was mainly established by the molecular data and has tiny morphological differences from small vannellids of the genera Vannella and Ripella. Among Vannella-like genera with no molecular data remain the genus Unda Schaeffer, 1926 and the genus Pessonella Pussard, 1973. These amoebae were never reliably re-isolated; the strain designated as Unda schaefferi Sawyer, 1975, represented with the strain ATCC 50810 used by Tekle and Wood (2017) and Kang et al. (2017) requires taxonomic study before be recognised as a distinct genus. In the above-mentioned papers, it groups with species of the genus Vannella.

During the study of the diversity of terrestrial lobose amoeba, we isolated the strain labelled as Van79. This strain had remarkable dorsal folds and longitudinal ridges and was initially misidentified as a representative of the genus Thecamoeba. Nevertheless, some morphological characters, together with molecular data, reliably grouped it with amoebae of the genus Vannella. Here we provide a morphological description of this unusual amoeba and results of molecular phylogenetic analysis.

Section snippets

Isolation and light microscopy

Strain Van79, which is the subject of the present paper was isolated from the sample containing dead plant remnants and leaves in the Kislovodsk town (Russia, 43°53′56.7″N 42°44′17.4″E). To isolate cells, tiny (2–4 mm across) pieces of collected substratum were placed in sterile 60 mm Petri dishes filled with wMY agar (Spiegel et al. 1995). Cells were cloned by cutting off tiny fragments of the agar containing the single amoeba cell, well isolated from others. These agar fragments were

Light microscopy

Locomotive cells of the strain Van79 were flattened, semi-circular, fan-shaped, spatulate, or had elongate outlines. Cells moved as a whole without forming discrete pseudopodia (Figs. 1A–J) and may be characterised as demonstrating fan-shaped, striate or rugose morphotype (Smirnov and Goodkov 1999; Smirnov and Brown 2004). In locomotion, cells show a wide frontal area of the hyaloplasm, sometimes extended to the lateral parts of the cell and forming an anterolateral hyaline crescent (Fig. 1D,

Strain Van79 represents a new species – Vannella primoblina n. sp

At the first glance, when using light microscopy methods, cells of the strain Van79 resemble representatives of the genus Thecamoeba. They often have elongated outlines and well-visible ridges and folds on the dorsal surface of the cell. These characters are usual for rugose thecamoebids (Dyková and Kostka 2013; Page 1977, 1988; Page and Siemensma 1991; Smirnov and Brown 2004; Smirnov and Goodkov 1999). However, careful observations show that moving cells often adopt fan-like or spatulate shape

Author contributions

All authors contributed equally to the present study and writing of the paper.

Acknowledgements

Supported by the Russian Science Foundation project № 20-14-00195 (species description, molecular studies and phylogeny, data analysis) and RFBR 19-04-01147 grant (concept, fieldwork, isolation of species, DNA isolation). The present study utilized equipment of the Core facility centers “Development of molecular and cell technologies” and “Culture Collection of microorganisms” of Saint Petersburg State University. We are grateful to Votinova Valentina for her help in collecting a sample that

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