The mixoplankton green Noctiluca scintillans (gNoctiluca) is known to form extensive green tides in tropical coastal ecosystems prone to eutrophication. In the Arabian Sea, their recent appearance and annual recurrence have upended an ecosystem that was once exclusively dominated by diatoms. Despite evidence of strong links to eutrophication, hypoxia and warming, the mechanisms underlying outbreaks of this mixoplanktonic dinoflagellate remain uncertain. Here we have used eco-physiological measurements and transcriptomic profiling to ascribe gNoctiluca’s explosive growth during bloom formation to the form of sexual reproduction that produces numerous gametes. Rapid growth of gNoctiluca coincided with active ammonium and phosphate release from gNoctiluca cells, which exhibited high transcriptional activity of phagocytosis and metabolism generating ammonium. This grazing-driven nutrient flow ostensibly promotes the growth of phytoplankton as prey and offers positive support successively for bloom formation and maintenance. We also provide the first evidence that the host gNoctiluca cell could be manipulating growth of its endosymbiont population in order to exploit their photosynthetic products and meet critical energy needs. These findings illuminate gNoctiluca’s little known nutritional and reproductive strategies that facilitate its ability to form intense and expansive gNoctiluca blooms to the detriment of regional water, food and the socio-economic security in several tropical countries.
Note: When clicking on a Digital Object Identifier (DOI) number, you will be taken to an external site maintained by the publisher.
Some full text articles may not yet be available without a charge during the embargo (administrative interval).
What is a DOI Number?
Some links on this page may take you to non-federal websites. Their policies may differ from this site.
-
None (Ed.)
Abstract -
Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.more » « less
-
Abstract 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.
-
Proliferating cell nuclear antigen (
PCNA ) plays critical roles in eukaryoticDNA replication and replication‐associated processes. It is typically encoded by one or two gene copies (pcna ) in eukaryotic genomes. Recently reported higher copy numbers ofpcna in some dinoflagellates raised a question of how this gene has uniquely evolved in this phylum. Through real‐timePCR quantification, we found a wide range ofpcna copy number (2–287 copies) in 11 dinoflagellate species (n = 38), and a strong positive correlation betweenpcna copy number and genome size (log10–log10transformed). Intraspecificpcna diverged up to 21% and are dominated by nonsynonymous substitutions, indicating strong purifying selection pressure on and hence functional necessity of this gene. By surveyingpcna copy numbers in eukaryotes, we observed a genome size threshold at 4 pgDNA , above which more than twopcna copies are found. To examine whether retrotransposition is a mechanism ofpcna duplication, we measured the copy number of retroposedpcna , taking advantage of the 22‐nt dinoflagellate‐specific spliced leader (DinoSL ) capping the 5′ end of dinoflagellate nuclear‐encodedmRNA s, which would exist in the upstream region of a retroposed gene copy. We found that retroposedpcna copy number increased with totalpcna copy number and genome size. These results indicate co‐evolution of dinoflagellatepcna copy number with genome size, and retroposition as a major mechanism ofpcna duplication in dinoflagellates. Furthermore, we posit that the demand of faithful replication and maintenance of the large dinoflagellate genomes might have favored the preservation of the retroposedpcna as functional genes. -
The planktonic dinoflagellate
Ptychodiscus noctiluca combined distinctive morphological features such as a disk‐shaped anteroposteriorly compressed cell body and an apical carina, together with a flexible and tough cell covering, suggesting intermediate characteristics between thecate and naked dinoflagellates.Ptychodiscus noctiluca was examined by light, epifluorescence, and scanning electron microscopy from specimens collected in the Mediterranean Sea and the North and South Atlantic Ocean.Ptychodiscus noctiluca showed a straight apical groove that bisected the carina, a cell covering with a polygonal surface reticulum, nucleus without capsule, sulcal intrusion in the episome, sulcal ventral flange, and yellowish‐green chloroplasts that are shared characters withBrachidinium /Karenia . The cell division was the typical binary fission of gymnodinioid dinoflagellates, although exceptionally in an oblique transversal axis. We examined the intraspecific variability during incubation experiments. In the fattened cells, termed asPtychodiscus carinatus , chloroplasts transformed into dark granules, and the cell acquired the swollen and smaller stage, termed asP. inflatus .Ptychodiscus carinatus ,P. inflatus, andDiplocystis antarctica are synonyms ofP. noctiluca . Molecular phylogeny based on theSSU rDNA sequence revealed thatPtychodiscus branched within the short‐branching dinokaryotic dinoflagellates as an independent lineage with affinity toBrachidinium/Karenia andKarlodinium /Takayama in a generally poorly resolved clade. Our results indicated that the order Ptychodiscales, established for unarmored dinoflagellates with a strongly developed pellicle, has artificially grouped thecate dinoflagellates (Kolkwitziella ,Herdmania ), naked dinoflagellates with thick cell covering (Balechina ,Cucumeridinium ) and other insufficiently known unarmored genera with typical cell coverings (Brachidinium ,Ceratoperidinium ).