Molecular Data Reveal a Cryptic Diversity in the Genus Urotricha (Alveolata, Ciliophora, Prostomatida), a Key Player in Freshwater Lakes, With Remarks on Morphology, Food Preferences, and Distribution.

Daniela Frantal,Michael Gruber,Daniela Beisser,Birgit Weißenbacher,Ulrike Scheffel,Sabine Filker,Laura Nachbaur,Thorsten Stoeck,Tatyana Darienko,Bettina Sonntag,Jens Boenigk,Kuimei Qian,Gianna Dirren-Pitsch,Sabine Agatha,Barbara Kammerlander,Thomas Pröschold

doi:10.3389/fmicb.2021.787290

Abstract

Species of the ciliate genus Urotricha are key players in freshwater plankton communities. In the pelagial of lakes, about 20 urotrich species occur throughout an annual cycle, some of which play a pivotal role in aquatic food webs. For example, during the phytoplankton spring bloom, they consume a remarkable proportion of the algal production. In ecological studies, urotrich ciliates are usually merely identified to genus rank and grouped into size classes. This is unsatisfying considering the distinct autecological properties of individual species and their specific spatial and temporal distribution patterns. As a basis for future research, we characterized in detail four common urotrich morphotypes, i.e., specimens identified as U. furcata and tentatively as U. agilis, U. pseudofurcata, and U. castalia, using state-of-the-art methods. We used an integrative polyphasic approach, in which morphological studies (in vivo observation, silver staining methods, scanning electron microscopy) were linked with a molecular approach exploiting four different gene fragments as taxonomic DNA barcodes with different resolution potential (SSU rDNA, ITS-1, ITS-2, hypervariable V4 and V9 regions of the SSU rDNA). We shed light on the diversity of urotrich ciliates as well as on their global distribution patterns, and annual cycles. Additionally, we coupled individual species occurrences and environmental parameters, and subsequently modeled the distribution and occurrence, using logistic regressions. Furthermore, for one strain putatively identified as U. castalia, we ascertained the optimal cultivation media and food preferences. Thereby, our comprehensive view on these important freshwater ciliates that frequently occur in environmental high throughput sequencing datasets worldwide will allow future studies to better exploit protistan plankton data from lakes.

Highlights

Members of the genus Urotricha Claparède and Lachmann, 1859 represent some of the most common planktonic ciliates in freshwater systems worldwide, including temperate and remote lakes, and reservoirs (e.g., Weisse et al, 1990; Sonntag et al, 2006, 2017; Sichrowsky et al, 2014; Posch et al, 2015; Kammerlander et al, 2016; Šimek et al, 2019)
The results revealed that U. castalia was feeding only on the mobile alga SAG 26.80 Cryptomonas sp., while not on immobile food items (MS-2017/1 Coelastrum sp., MS-2017/2 Choricystis sp., MS-2017/8 Cosmarium sp., and MS-2017/7 Acutodesmus obliquus; Supplementary Figures 1, 3)
The unique conical cell shape was used by Penard (1922) and Kahl (1930) for identifying the species, which has been redescribed from life and after silver staining by Foissner (1979); further, it had been included in two taxonomic and ecological monographs on freshwater ciliates (Foissner et al, 1994, 1999)

Summary

Introduction

Members of the genus Urotricha Claparède and Lachmann, 1859 represent some of the most common planktonic ciliates in freshwater systems worldwide, including temperate and remote lakes, and reservoirs (e.g., Weisse et al, 1990; Sonntag et al, 2006, 2017; Sichrowsky et al, 2014; Posch et al, 2015; Kammerlander et al, 2016; Šimek et al, 2019). Urotricha species often dominate ciliate communities and co-occur with other small prostomatids, such as Balanion planctonicum, halteriids, and diverse oligotrichs, e.g., Rimostrombidium species. Species of this genus are considered omnivores with a preference for algae. They significantly foster the clear-water phase after the algal spring bloom in temperate lakes (Weisse et al, 1990; Foissner et al, 1999; Sonntag et al, 2006; Tirok and Gaedke, 2006). The role of ciliates in the planktonic food web, including predators and algae, is largely a black box, though ciliate grazing on phytoplankton contributes significantly to the carbon flux. For a better understanding of the role of ciliates within the planktonic food web, investigations on a large variety of predator-prey relationships are needed

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