DNA metabarcoding reveals vertical variation and hidden diversity of Alveolata and Rhizaria communities in the western North Pacific

Sogawa, Sayaka; Nakamura, Yasuhide; Nagai, Satoshi; Nishi, Noriko; Hidaka, Koichi; Shimizu, Yoshihisa; Setou, Takashi

doi:10.1016/j.dsr.2022.103765

Cited by 7 publications

(7 citation statements)

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“…This pattern is likely explained by abiotic and biotic factors that correlate with depth; for example, in our study, depth was negatively related to temperature, salinity, oxygen, and fluorescence. This is in general agreement with changes in productivity and overall environmental conditions known to affect protist alpha-diversity in the vertical profile, especially from photic to aphotic waters (Blanco-Bercial et al, 2022;Schnetzer et al, 2011;Sogawa et al, 2022).…”

Section: Discussionsupporting

confidence: 86%

“…Much less is known about ciliate taxa and their potential activities (bacterivory, detritivory, parasitism) in deeper waters, where sharp changes in major environmental factors (e.g. light, temperature, oxygen, food resources) are known to affect the diversity and composition of broader protist communities (Blanco‐Bercial et al, 2022; Ollison et al, 2021; Schnetzer et al, 2011; Sogawa et al, 2022). This causes a biased view of ciliate contributions to the functioning of marine ecosystems, where these and other protists greatly influence productivity and biogeochemistry (Worden et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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The photic‐aphotic divide is a strong ecological and evolutionary force determining the distribution of ciliates (Alveolata, Ciliophora) in the ocean

Santoferrara

Qureshi

Sher

et al. 2023

J Eukaryotic Microbiology

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The bulk of knowledge on marine ciliates is from shallow and/or sunlit waters. We studied ciliate diversity and distribution across epi‐ and mesopelagic oceanic waters, using DNA metabarcoding and phylogeny‐based metrics. We analyzed sequences of the 18S rRNA gene (V4 region) from 369 samples collected at 12 depths (0–1000 m) at the Bermuda Atlantic Time‐series Study site of the Sargasso Sea (North Atlantic) monthly for 3 years. The comprehensive depth and temporal resolutions analyzed led to three main findings. First, there was a gradual but significant decrease in alpha‐diversity (based on Faith's phylogenetic diversity index) from surface to 1000‐m waters. Second, multivariate analyses of beta‐diversity (based on UniFrac distances) indicate that ciliate assemblages change significantly from photic to aphotic waters, with a switch from Oligotrichea to Oligohymenophorea prevalence. Third, phylogenetic placement of sequence variants and clade‐level correlations (EPA‐ng and GAPPA algorithms) show Oligotrichea, Litostomatea, Prostomatea, and Phyllopharyngea as anti‐correlated with depth, while Oligohymenophorea (especially Apostomatia) have a direct relationship with depth. Two enigmatic environmental clades include either prevalent variants widely distributed in aphotic layers (the Oligohymenophorea OLIGO5) or subclades differentially distributed in photic versus aphotic waters (the Discotrichidae NASSO1). These results settle contradictory relationships between ciliate alpha‐diversity and depth reported before, suggest functional changes in ciliate assemblages from photic to aphotic waters (with the prevalence of algivory and mixotrophy vs. omnivory and parasitism, respectively), and indicate that contemporary taxon distributions in the vertical profile have been strongly influenced by evolutionary processes. Integration of DNA sequences with organismal data (microscopy, functional experiments) and development of databases that link these sources of information remain as major tasks to better understand ciliate diversity, ecological roles, and evolution in the ocean.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

The photic‐aphotic divide is a strong ecological and evolutionary force determining the distribution of ciliates (Alveolata, Ciliophora) in the ocean

Santoferrara

Qureshi

Sher

et al. 2023

J Eukaryotic Microbiology

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“…The most interesting example is represented by Syndiniales, a group of species that spend part of their life cycle as parasites of other dinoflagellates, protists or marine invertebrates, while their free stages are not identifiable with optical methods. The great diversity of this group has been acknowledged only in recent decades thanks to molecular approaches, which have also revealed their abundance in the natural environment in both open oceanic and coastal areas (e.g., Anderson & Harvey, 2020; Armeli Minicante et al, 2019; Clarke et al, 2019; Guillou et al, 2008; Gutierrez‐Rodriguez et al, 2022; Sehein et al, 2022; Sogawa et al, 2022). The high‐relative abundance of Syndiniales in the winter months in the Gulf of Naples was already noticed in a previous study, where this group of Alveolata accounted for about 50% of the protist community in December (Piredda et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Metabarcoding reveals marked seasonality and a distinctive winter assemblage of dinoflagellates at a coastal LTER site in the Gulf of Naples

et al. 2023

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Dinoflagellates constitute an abundant and diversified component of marine plankton, mostly associated with stratified conditions typical of late spring through autumn in temperate regions. Yet, difficulties with the identification of many species limit the knowledge of their composition and seasonal succession. Here we use a 3‐year V4‐18S rDNA metabarcoding dataset (4,366,007 reads, 4650 Amplicon Sequence Variants, ASVs) collected on 48 dates at the Long‐Term Ecological Research site MareChiara (LTER–MC) to explore the diversity and temporal distribution of dinoflagellates in the Gulf of Naples (Mediterranean Sea). A large fraction of dinoflagellate ASVs (55%, 68% of the reads) were assigned to 187 species in 85 genera, while 33% (23% of the reads) were attributed to undetermined Syndiniales, and the remainder to unidentified groups. A total of 147 ASVs were assigned at 100% similarity to 135 reference sequences, corresponding to 116 species, 46 of which were putative new records for the Gulf of Naples. Cluster analysis conducted on a normalized dataset of 1199 ASVs identified four sample clusters that corresponded largely to the spring, summer, autumn and winter seasons, respectively, each including samples from all 3 years. Syndiniales were particularly abundant (43.1%) in the winter cluster, whereas Gyrodinium reached higher percentages in the summer and autumn ones (38.6% and 57.8%), Gymnodiniales sensu stricto were more abundant in spring (11.5%) and Gonyaulacales in summer (13.5%). Almost half of the ASVs analysed (561) were significantly associated with one of the four seasonal clusters (p < .05). The winter group of ASVs was particularly rich (348 ASVs) and mainly consisted of naked and parasitic taxa, which are impossible to identify in routine phytoplankton observations in light microscopy. Despite biases mainly ascribed to both the incompleteness of the reference dataset and the limited resolution of the marker gene, the metabarcoding approach has provided new insights into the ecology and distribution of this important component of the plankton, highlighting its marked seasonality along with the existence of a diversified and previously overlooked dinoflagellate community in winter.

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“…The biological interactions (e.g., competition, predator–prey relationships and symbiosis, including parasitism) of protists have been widely studied, mainly focusing on ‘culturable’ species in the domain of microbiology or protistology. However, many protists in natural environments cannot be successfully cultured under artificial conditions, and these ‘difficult‐to‐culture’ protists are reported to play important roles in natural environments (Biard et al, 2016; Ikenoue et al, 2019; Sogawa et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…These two groups are heterotrophic or mixotrophic unicellular zooplankton, most of which have siliceous skeletons. They are thought to be key groups in ecosystems and material cycles in the world ocean because their high abundance and large contribution to material cycles have often been reported in the past decade (Biard & Ohman, 2020; Nakamura et al, 2013; Sogawa et al, 2022). The symbiosis between these two groups and other eukaryotic organisms has also attracted attention recently.…”

Section: Introductionmentioning

confidence: 99%

DNA metabarcoding focused on difficult‐to‐culture protists: An effective approach to clarify biological interactions

Nakamura,

Itagaki,

Tuji

et al. 2023

Environmental Microbiology

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DNA metabarcoding on a single organism is a promising approach to clarify the biological interactions (e.g., predator–prey relationships and symbiosis, including parasitism) of difficult‐to‐culture protists. To evaluate the effectiveness of this method, Radiolaria and Phaeodaria, which are ecologically important protistan groups, were chosen as target taxa. DNA metabarcoding on a single organism focused on the V9 region of the 18S rRNA gene revealed potential symbionts, parasites and food sources of Radiolaria and Phaeodaria. Previously reported hosts and symbionts (parasites) were detected, and newly recognized combinations were also identified. The contained organisms largely differed between Radiolaria and Phaeodaria. In Radiolaria, members of the same order tended to contain similar organisms, and the taxonomic composition of possible symbionts, parasites, and food sources was fixed at the species level. Members of the same phaeodarian family, however, did not contain similar organisms, and body part (i.e., the central capsule or the phaeodium) was the most important factor that divided the taxonomic composition of detected organisms, implying that the selection of appropriate body part is important when trying to ascertain contained organisms, even for unicellular zooplankton. Our results show that DNA metabarcoding on a single organism is effective in revealing the biological interactions of difficult‐to‐culture protists.

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DNA metabarcoding reveals vertical variation and hidden diversity of Alveolata and Rhizaria communities in the western North Pacific

Cited by 7 publications

References 58 publications

The photic‐aphotic divide is a strong ecological and evolutionary force determining the distribution of ciliates (Alveolata, Ciliophora) in the ocean

The photic‐aphotic divide is a strong ecological and evolutionary force determining the distribution of ciliates (Alveolata, Ciliophora) in the ocean

Metabarcoding reveals marked seasonality and a distinctive winter assemblage of dinoflagellates at a coastal LTER site in the Gulf of Naples

DNA metabarcoding focused on difficult‐to‐culture protists: An effective approach to clarify biological interactions

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