Summary
Benthic microeukaryotes are key ecosystem drivers in marine sandy beaches, an important and dynamic environment; however, little is known about their diversity and biogeography on a large ...spatial scale. Here, we investigated the community composition and geographical distributions of benthic microeukaryotes using high‐throughput sequencing of the 18S rRNA gene and quantified the contributions of environmental factors and spatial separation on the distribution patterns of both rare and abundant taxa. We collected 36 intertidal samples at 12 sandy beaches from four regions that spanned distances from 0.001 to 12,000 km. We found 12,890 operational taxonomic units (OTUs; 97% sequence identity level) including members of all eukaryotic super‐groups and several phyla of uncertain position. Arthropoda and Diatomeae dominated the sequence reads in abundance, but Ciliophora and Discoba were the most diverse groups across all samples. About one‐third of the OTUs could not be definitively classified at a similarity level of 80%, supporting the view that a large number of rare and minute marine species may have escaped previous characterization. We found generally similar geographical patterns for abundant and rare microeukaryotic sub‐communities, and both showed a significant distance–decay similarity trend. Variation partitioning showed that both rare and abundant sub‐communities exhibited a slightly stronger response to environmental factors than spatial (distance) factors. However, the abundant sub‐community was strongly correlated with variations in spatial, environmental and sediment grain size factors (66% of variance explained), but the rare assemblage was not (16%). This suggests that different or more complex mechanisms generate and maintain diversity in the rare biosphere in this habitat.
The relative importance of different ecological processes that shape community structure is a central but poorly understood topic in protist ecology. This study used an 18S rRNA gene sequencing ...approach to examine the relative contributions of environmental selective (environmental filtering) and neutral processes (dispersal and ecological drift) in the community assembly of three diverse protist groups (Bacillariophyta, Cercozoa, and Ciliophora) from intertidal sediment samples spanning a geographical distance up to 12,000 km. All three protist communities exhibited similar and distinct biogeographical patterns, and followed strong distance–decay relationships at continental scale (ca. 12,000 km), regional scale (ca. 1500 km), and local scale (ca. 50 km). Network analysis showed that temperature, salinity, nitrite and nitrate nitrogen, total nitrogen, and 0.1–0.25 mm grain size together associated with 60.8%, 55.5%, and 50.0% of the OTUs, which represented 68.1%, 58.5%, and 59.2% of sequence abundances for Bacillariophyta, Cercozoa, and Ciliophora co-occurrence networks, respectively, indicating that these environmental variables played the central roles in influencing community composition. On the other hand, a neutral community model explained 73.6%, 64.2%, and 70.2% of community variation for Bacillariophyta, Cercozoa, and Ciliophora, respectively. More importantly, variation partitioning and partial Mantel tests showed that environmental selection exhibited a slightly greater influence on Ciliophora compared to spatial factors, but both components were roughly equivalent in Bacillariophyta and Cercozoa communities. Taken together, these results demonstrate that both environmental selection and neutral processes play important roles in creating the biogeographical patterns of protist communities in intertidal sandy beach ecosystems.
Ciliates are abundant microplankton that are widely distributed in the ocean. In this paper, the distribution patterns of ciliate diversity in the South China Sea (SCS) were analyzed by compiling ...community data from previous publications. Based on morphological identification, a total of 592 ciliate species have been recorded in the SCS. The ciliate communities in intertidal, neritic and oceanic water areas were compared in terms of taxonomy, motility and feeding habit composition, respectively. Significant community variation was revealed among the three areas, but the difference between the intertidal area and the other two areas was more significant than that between neritic and oceanic areas. The distributions of ciliates within each of the three areas were also analyzed. In the intertidal water, the community was not significantly different among sites but did differ among habitat types. In neritic and oceanic areas, the spatial variation of communities among different sites was clearly observed. Comparison of communities by taxonomic and ecological traits (motility and feeding habit) indicated that these traits similarly revealed the geographical pattern of ciliates on a large scale in the SCS, but to distinguish the community variation on a local scale, taxonomic traits has higher resolution than ecological traits. In addition, we assessed the relative influences of environmental and spatial factors on assembly of ciliate communities in the SCS and found that environmental selection is the major process structuring the taxonomic composition in intertidal water, while spatial processes played significant roles in influencing the taxonomic composition in neritic and oceanic water. Among ecological traits, environmental selection had the most important impact on distributions.
Mesodinium rubrumis a globally distributed nontoxic ciliate that is known to produce intense red-colored blooms using enslaved chloroplasts from its algal prey. Although frequent enough to have been ...observed by Darwin, blooms ofM. rubrumare notoriously difficult to quantify becauseM. rubrumcan aggregate into massive clouds of rusty-red water in a very short time due to its high growth rates and rapid swimming behavior and can disaggregate just as quickly by vertical or horizontal dispersion. A September 2012 hyperspectral image from the Hyperspectral Imager for the Coastal Ocean sensor aboard the International Space Station captured a dense red tide ofM. rubrum(10⁶ cells per liter) in surface waters of western Long Island Sound. Genetic data confirmed the identity of the chloroplast as a cryptophyte that was actively photosynthesizing. Microscopy indicated extremely high abundance of its yellow fluorescing signature pigment phycoerythrin. Spectral absorption and fluorescence features were related to ancillary photosynthetic pigments unique to this organism that cannot be observed with traditional satellites. Cell abundance was estimated at a resolution of 100 m using an algorithm based on the distinctive yellow fluorescence of phycoerythrin. Future development of hyperspectral satellites will allow for better enumeration of bloom-forming coastal plankton, the associated physical mechanisms, and contributions to marine productivity.
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•New sequencing of 27 species and curation of all GenBank sequences for three rDNA loci.•Concatenated phylogeny with 18 families and updated classification with 23 families.•Favella ...forms a distinct family and Tintinnopsis is spread among 11 lineages.•A previously-unknown environmental clade matches Leegaardiellidae.•Prevalence of uncharacterized and cryptic diversity in aloricates.
Ciliated protists in the subclasses Choreotrichia and Oligotrichia are major components of marine plankton. Despite their ecological relevance, there are uncertainties in their systematics and diversity. We retrieved and curated all the GenBank ribosomal DNA (rDNA) sequences from these groups, which were analyzed in two ways. The first approach was based on morphologically-identified sequences (including those of two families and six genera newly studied here by single-cell sequencing), and aimed at improving phylogenetic inferences using concatenated sequences of three rDNA loci. Based on phylogenetic and morphological support, we update the taxonomic classification of these subclasses into 23 families, including the re-established Favellidae. We also propose an informal naming system for incertae sedis taxa, namely Tintinnopsis and five related genera that are spread among eleven lineages. The second approach included unidentified environmental sequences, and was used to explore potentially novel diversity in these subclasses. Our results support high proportions of both synonyms in tintinnids and uncharacterized taxa in choreotrichids and oligotrichs. One previously unidentified, environmental clade is here linked to our new Leegaardiellidae sequences. Our curation of almost 4000 rDNA sequences exemplifies known issues of public repositories, and suggests caution in both the use and contribution to these unique resources for evolutionary and diversity studies.
Abstract
Tintinnid ciliates are suitable models to study the diversity and biogeography of microbial plankton. In addition to morphological data accumulated over two centuries, most known families ...and common genera have been linked to DNA sequences in relatively recent barcoding efforts. This backbone of morphologically identified sequences is used here to classify environmental sequences in order to study global and local spatial trends. Analyses of tintinnid SSU rDNA data collected worldwide (about 900 sequences available in NCBI GenBank) and in the northwest Atlantic Ocean (about 500,000 sequences obtained by metabarcoding) support distribution patterns related to salinity, bathymetry and climate/ latitude. In addition to the marine–freshwater dichotomy and a pattern of coastal-only taxa known for tintinnids, there is a global trend of phylotypes restricted to brackish or open waters. Local alpha and beta diversity analyses show that assemblage differences among estuarine, coastal and open waters are not significant regarding richness, but are significant in terms of phylogenetic composition. We also confirm spatial restriction of boreal and austral taxa, and stress that cosmopolitanism cannot be assessed by molecular methods that lump data from potentially endemic and commonly widespread taxa. Heterogeneous diversity, biogeography and phylogenetic resolution within and among tintinnid lineages raise questions about the processes that promote their diversification and determine their spatial distributions.
Although protists (microbial eukaryotes) provide an important link between bacteria and Metazoa in food webs, we do not yet have a clear understanding of the spatial scales on which protist diversity ...varies. Here, we use a combination of DNA fingerprinting (denaturant gradient gel electrophoresis or DGGE) and high-throughput sequencing (HTS) to assess the ciliate community in the class Spirotrichea at varying scales of 1-3 km sampled in three locations separated by at least 25 km-offshore, midshelf and inshore-along the New England shelf. Analyses of both abundant community (DGGE) and the total community (HTS) members reveal that: 1) ciliate communities are patchily distributed inshore (i.e. the middle station of a transect is distinct from its two neighboring stations), whereas communities are more homogeneous among samples within the midshelf and offshore stations; 2) a ciliate closely related to Pelagostrobilidium paraepacrum 'blooms' inshore and; 3) environmental factors may differentially impact the distributions of individual ciliates (i.e. OTUs) rather than the community as a whole as OTUs tend to show distinct biogeographies (e.g. some OTUs are restricted to the offshore locations, some to the surface, etc.). Together, these data show the complexity underlying the spatial distributions of marine protists, and suggest that biogeography may be a property of ciliate species rather than communities.
We used an experimental approach of analyzing marine microcosms to evaluate the impact of both predation (top-down) and food resources (bottom-up) on spirotrich ciliate communities. To assess the ...diversity, we used two molecular methods-denaturing gradient gel electrophoresis (DGGE) and high-throughput sequencing (HTS). We carried out two types of experiments to measure top-down (adult copepods as predators) and bottom-up effects (phytoplankton as food resources) on the spirotrich ciliates. We observed both strong incubation effects (untreated controls departed from initial assessment of diversity) and high variability across replicates within treatments, particularly for the bottom-up experiments. This suggests a rapid community turn-over during incubation and differential susceptibility to the effects of experimental manipulation. Despite the variability, our analyses reveal some broad patterns such as (1) increasing adult copepod predator abundance had a greater impact on spirotrich ciliates than on other microbial eukaryotes; (2) there was no evidence for strong food selection by the dominant spirotrich ciliates.
Marine microbial eukaryotes play critical roles in planktonic food webs and have been described as most diverse in the photic zone where productivity is high. We used high‐throughput sequencing (HTS) ...to analyse the spatial distribution of planktonic ciliate diversity from shallow waters (<30 m depth) to beyond the continental shelf (>800 m depth) along a 163 km transect off the coast of New England, USA. We focus on ciliates in the subclasses Oligotrichia and Choreotrichia (class Spirotrichea), as these taxa are major components of marine food webs. We did not observe the decrease of diversity below the photic zone expected based on productivity and previous analyses. Instead, we saw an increase of diversity with depth. We also observed that the ciliate communities assessed by HTS cluster by depth layer and degree of water column stratification, suggesting that community assembly is driven by environmental factors. Across our samples, abundant OTUs tend to match previously characterized morphospecies while rare OTUs are more often undescribed, consistent with the idea that species in the rare biosphere remain to be characterized by microscopy. Finally, samples taken below the photic zone also reveal the prevalence of two uncharacterized (i.e. lacking sequenced morphospecies) clades – clusters X1 and X2 – that are enriched within the nano‐sized fraction (2–10 μm) and are defined by deletions within the region of the SSU‐rDNA analysed here. Together, these data reinforce that we still have much to learn about microbial diversity in marine ecosystems, especially in deep‐waters that may be a reservoir for rare species and uncharacterized taxa.
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