Metatranscriptome Profiling Indicates Size-Dependent Differentiation in Plastic and Conserved Community Traits and Functional Diversification in Dinoflagellate Communities

Abstract

Communities of microscopic dinoflagellates are omnipresent in aquatic ecosystems. Consequently, their traits drive community processes with profound effects on global biogeochemistry. Species traits are, however, not necessarily static but respond to environmental changes in order to maintain fitness and may differ with cell size that scales physiological rates. Comprehending such trait characteristics is necessary for a mechanistic understanding of plankton community dynamics and resulting biogeochemical impacts. Here, we used information theory to analyze metatranscriptomes of micro-and nano-dinoflagellate communities in three ecosystems. Measures of gene expression variations were set as a proxy to determine conserved and plastic community traits and the environmental influence on trait changes. Using metabarcoding, we further investigated if communities with a more similar taxon composition also express more similar traits. Our results indicate that plastic community traits mainly arise from membrane vesicle associated processes in all the environments we investigated. A specific environmental influence on trait plasticity was observed to arise from nitrogen availability in both size classes. Species interactions also appeared to be responsible for trait plasticity in the smaller-sized dinoflagellates. Additionally, the smaller-sized dinoflagellate communities are characterized by the expression of a large pool of habitat specific genes despite being taxonomically more similar across the habitats, in contrast to the microplanktonic assemblages that adapted to their environments by changing species composition. Our data highlight the functional diversification on the gene level as a signature of smaller sized dinoflagellates, nitrogen availability and species interactions as drivers of trait plasticity, and traits most likely linked to fitness and community performance.

Functional Genomics Differentiate Inherent and Environmentally Influenced Traits in Dinoflagellate and Diatom Communities

“…For the biologic KEGG category genetic information processing (folding, sorting and degradation), dinoflagellates highly correlated to SNARE interactions in vesicular transport (SNARE: SNP-Receptor, Soluble N-ethylmaleimide sensitive fusion attachment protein receptor). Pathways related to the uptake and secretion of substances (intracellular trafficking, secretion and vesicular transport; KOG-Category 'U') were also identified in a metatranscriptomics study by Wohlrab et al [23] as particularly important for the persistence of dinoflagellate communities. Also, important are processes associated with the excretion or uptake of substances that can have profound effects on community members and biogeochemical processes (e.g., the secretion of allelochemically active molecules).…”

“…Yet dinoflagellates include autotrophic, heterotrophic, parasitic and endosymbiotic species, thus encompassing diverse ecological niches. Differences in the life strategies and nutrition modes of these two groups should be detectable in their expressed genes, as identified for diatoms [22], dinoflagellates [23,24] or both groups [25,26]. However, microeukaryotes are regulated by the interplay of individual species traits, biotic interactions and the environment [15] and these interacting challenges render it difficult to identify specific trophic roles.…”

“…The detailed knowledge generated in the laboratory allows for the transfer of gene expression analyses into field studies, e.g., to assess more complex community structures [32] and reveal aspects of global biogeography of eukaryotic genes [33]. Metatranscriptomic studies have already contributed significantly to our understanding of the biology of diatoms and dinoflagellates-from genes to ecosystems-and have provided other new insights into niche partitioning and resource use of diatoms [22,34], the impact of abiotic factors on community structure [26,35,36], mechanisms potentially governing diatom and dinoflagellate dominance [25], size-dependency of plastic and conserved community traits of dinoflagellates [23] and the tight circadian-regulated metabolic coupling within marine microbial communities [37]. To improve our understanding of the interplay between taxonomic and functional diversity of a community relative to environmental influence, this study distinguishes functional processes that may be affected by changing environmental conditions from those functions that are affected by biodiversity (species identity).…”

Resource Partitioning Between Phytoplankton and Bacteria in the Coastal Baltic Sea

“…ciliates (Oligotrichia, Choreotrichia) along with primarily heterotrophic bacteria [Actinobacteria (Microbacteriaceae, Sporichthyaceae), Bacteroidetes (Flavobacteriaceae, Cytophagaceae), Proteobacteria (Pseudomonadaceae, Pelagibacter, and Comamonadaceae)], in line with taxa frequently occurring in the Baltic Sea (Johansson et al, 2004;Riemann et al, 2008;Kremp et al, 2009;Herlemann et al, 2011;Wohlrab et al, 2018). Discrepancies in phytoplankton genus/taxa composition between light microscopy observations and 18S rRNA amplicon sequencing have been reported previously (Xiao et al, 2014) and illustrate the benefit of a combined approach.…”

Phylogenetic placement of environmental sequences using taxonomically reliable databases helps to rigorously assess dinophyte biodiversity in Bavarian lakes (Germany)

“…Trees such as that obtained in this study serve as a taxonomic scaffold for the systematic placement of newly generated dinophyte sequences, even if they are short as it is in the case of next-generation sequencing amplicons. Our approach to determine dinophyte species using reference trees as inferred from multi-locus rRNA alignments is proven successful to a certain degree, at least for samples from the freshwater environment (providing also some new dinophyte records for Bavaria: Table 2), but also from the marine realm (Elferink et al, 2017;Wohlrab et al, 2018 The most frequently encountered taxa correspond to those that are known from morphological surveys in Bavaria, which comprise Apocalathium (Mauch et al, 2003;Mischke, Riedmüller, Hoehn, Deneke, & Nixdorf, 2015;Schaumburg, 1996), Ceratium (Mauch et al, 2003;Raeder, 1990;Schaumburg, 1996;Schaumburg & Hehl, 2001),…”