First Molecular Characterization of the Elusive Marine Protist Meteora sporadica

Meteora sporadica is a protist species first described by Hausmann et al. (2002) in deep-sea sediments from the Sporades Basin, Eastern Mediterranean Sea. Due to its unusual morphology and locomotion, very different from those of other high-rank eukaryotic taxa, it was classified as an incertae sedis species. Unfortunately, its morphological characterization was not accompanied by the generation of molecular data, preventing its placement in molecular phylogenetic trees including other protist lineages. Here, we report the observation of protist cells in sediments from a shallow marine lagoon in the Mediterranean Sea with morphological characteristics indistinguishable from those of Meteora sporadica. Given this similarity and the geographical proximity to the type location, we consider that the organism that we observed likely corresponded to the type species, M. sporadica, which seems to be a benthic predator spanning from shallow to deep-sea habitats. We determined the 18S rRNA gene sequence of M. sporadica from micromanipulated cells. Searches in sequence databases did not yield closely related hits, suggesting that Meteora is a rare organism. Phylogenetic analyses did not show any close affinity with other eukaryotic groups, supporting its initial incertae sedis status and suggesting that it may define a new high-rank level eukaryotic lineage.

Introduction

Meteora sporadica is an extremely unusual protist that was first reported 20 years ago in deep sea sediment samples from the Sporades Basin in the Eastern Mediterranean Sea (Hausmann et al. 2002). It exhibited small colorless non-flagellated cells with an oval shape that measured 3.0–4.4 μm long and 2.0–4.0 μm wide. What made this protist truly unique were its unusual appendages and movement. Meteora glides on substrates using two types of appendages: two lateral arm-like appendages (one on each side of the equatorial plan of the cell), which present a continuous rowing movement, and two longer appendages, one on each pole of the cell, aligned in the direction of the cell movement. No other eukaryotic organism has ever been described to move in this peculiar way. It was hypothesized that the rowing movement of the two short arms enhances the chance to encounter bacterial prey, which is then immobilized by putative extrusome granules (up to 2 on each arm) (Hausmann et al. 2002).

Due to the striking morphological dissimilarity with members of all other known eukaryotic taxa, Meteora was classified as Protista incertae sedis. Unfortunately, the authors of the original description did not succeed to stablish a culture and no molecular data has been obtained for this species to date. In this study, we determined the 18S rRNA gene sequence of protist cells collected from sediment of a shallow marine lagoon in the Mediterranean island of Mljet (Croatia), which were morphologically indistinguishable from the previously described Meteora sporadica. The morphological similarity and geographical proximity between our sampling point and the type locality support the notion that the protist cells studied in this work correspond to the type species Meteora sporadica. The analysis of its 18S rRNA gene sequence allowed us to study its phylogeny, which showed its lack of close affinity with any other eukaryotic group, and its absence in environmental 18S rRNA gene sequence databases.