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Abstract
Ciliates represent central nodes in freshwater planktonic food webs, and many species show pronounced seasonality, with short-lived maxima of a few dominant taxa while many being rare or ephemeral. These observations are primarily based on morphospecies counting methods, which, however, have limitations concerning the amount and volume of samples that can be processed. For high sampling frequencies at large scales, high throughput sequencing (HTS) of freshwater ciliates seems to be a promising tool. However, several studies reported large discrepancy between species abundance determinations by molecular compared to morphological means. Therefore, we compared ciliate DNA metabarcodes (V9 regions of the 18S rRNA gene) with morphospecies counts for a 3-year study (Lake Zurich, Switzerland; biweekly sampling, n = 74). In addition, we isolated, cultivated and sequenced the 18S rRNA gene of twelve selected ciliate species that served as seeds for HTS analyses. This workflow allowed for a detailed comparison of V9 data with microscopic analyses by quantitative protargol staining (QPS). The dynamics of V9 read abundances over the seasonal cycle corroborated well with morphospecies population patterns. Annual successions of rare and ephemeral species were more adequately characterized by V9 reads than by QPS. However, numbers of species specific sequence reads only partly reflected rank orders seen by counts. In contrast, biomass-based assemblage compositions showed higher similarity to V9 read numbers, probably indicating a relation between cell sizes and numbers / sizes of macronuclei (or 18S rRNA operons). Full-length 18S rRNA sequences of ciliates assigned to certain morphospecies are urgently needed for barcoding approaches as planktonic taxa are still poorly represented in public databases and the interpretation of HTS data depends on profound reference sequences. Through linking operational taxonomic units (OTUs) with known morphospecies, we can use the deep knowledge about the autecology of these species.
Highlights
Seasonal successions of phyto- and metazooplankton often show predictive dynamics, which were described in a conceptual framework, the Plankton Ecology Group (PEG) model (Sommer et al, 1986)
The 5 L water volume of each sample was split in 300 mL for the morphospecies counting method and 4 L for high throughput sequencing (HTS), i.e., the analyzed water came from the same starting volume for both methods
Differences between the two methods were striking for some ciliates, e.g., specific reads for R. lacustris were recorded for all investigated samples (n = 74), but we found this species only in 50% of inspected quantitative protargol staining (QPS) preparations
Summary
Seasonal successions of phyto- and metazooplankton often show predictive dynamics, which were described in a conceptual framework, the Plankton Ecology Group (PEG) model (Sommer et al, 1986). Seasonal successions of ciliate assemblages and therein involved species have been well described for various temperate lakes (Beaver and Crisman, 1989; Müller et al, 1991; Carrias et al, 1998; Sonntag et al, 2006; Zingel and Nõges, 2010; see the extensive literature summary in Foissner et al, 1999) These studies have one common thread – their outcome is based on the identification and quantification of morphologically well-defined species (morphospecies, Foissner et al, 1999) via various microscopy techniques. Morphospecies counting allows for the quantification of abundances and biomasses per water volume, which is a prerequisite to study energy flows between trophic entities in lakes
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