Temporal changes in the ciliate assemblage and consecutive estimates of their grazing effect during the course of a Heterocapsa circularisquama bloom

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Specific toxic effect of dinoflagellate Heterocapsa circularisquama on the rotifer Brachionus plicatilis

Heterocapsa circularisquama (Dinophyceae), a noxious red tide dinoflagellate, is known to have a specifically lethal effect on shellfish, especially bivalves such as pearl oyster (Pinctada fucata), but no detrimental effects of this alga on fishes have not been observed so far. In this study, we found that H. circularisquama was toxic to a microzooplankton, a rotifer (Brachionus plicatilis) in a cell concentration-dependent manner, while the cultured supernatant or ultrasonic ruptured H. circularisquama had no significant toxic effect on the rotifer. Since no such toxic effects on the rotifer were observed in Chattonella marina, Heterosigma akashiwo, or Cochlodinium polykrikoides, other species of harmful red tide plankton, H. circularisquama may have a strictly specific toxic mechanism against the rotifer as well as bivalves.     

Growth characteristics and intraspecies host specificity of a large virus infecting the dinoflagellate Heterocapsa circularisquama

The growth characteristics and intraspecies host specificity of Heterocapsa circularisquama virus (HcV), a large icosahedral virus specifically infecting the bivalve-killing dinoflagellate H. circularisquama, were examined. Exponentially growing host cells were more sensitive to HcV than those in the stationary phase, and host cells were more susceptible to HcV infection in the culture when a higher percent of the culture was replaced with fresh medium each day, suggesting an intimate relationship between virus sensitivity and the physiological condition of the host cells. HcV was infective over a wide range of temperatures, 15 to 30 degrees C, and the latent period and burst size were estimated at 40 to 56 h and 1,800 to 2,440 infective particles, respectively. Transmission electron microscopy revealed that capsid formation began within 16 h postinfection, and mature virus particles appeared within 24 h postinfection at 20 degrees C. Compared to Heterosigma akashiwo virus, HcV was more widely infectious to H. circularisquama strains that had been independently isolated in the western part of Japan, and only 5.3% of the host-virus combinations (53 host and 10 viral strains) showed resistance to viral infection. The present results are helpful in understanding the ecology of algal host-virus systems in nature.     

Physiological and Optical Responses of the Harmful Dinoflagellate Heterocapsa circularisquama to a Range of Salinity

The responses of division rate, cell volume, cellular carbon (C) and nitrogen (N), cellular pigments and optical characteristics to changes in salinity were examined in the dinoflagellate Heterocapsa circularisquama. The physiological and optical characteristics of H. circularisquama were significantly affected by changes in salinity. When cells were exposed to different salinities, they exhibited physiological acclimation by adjusting their cellular properties associated with growth. This could be a beneficial tactic for ensuring proliferation and limiting damages induced by adverse environmental factors. The results of this study could be essential for assisting in the development of growth models for H. circularisquama.     

Growth Characteristics and Intraspecies Host Specificity of a Large Virus Infecting the Dinoflagellate Heterocapsa circularisquama

The growth characteristics and intraspecies host specificity of Heterocapsa circularisquama virus (HcV), a large icosahedral virus specifically infecting the bivalve-killing dinoflagellate H. circularisquama, were examined. Exponentially growing host cells were more sensitive to HcV than those in the stationary phase, and host cells were more susceptible to HcV infection in the culture when a higher percent of the culture was replaced with fresh medium each day, suggesting an intimate relationship between virus sensitivity and the physiological condition of the host cells. HcV was infective over a wide range of temperatures, 15 to 30°C, and the latent period and burst size were estimated at 40 to 56 h and 1,800 to 2,440 infective particles, respectively. Transmission electron microscopy revealed that capsid formation began within 16 h postinfection, and mature virus particles appeared within 24 h postinfection at 20°C. Compared to Heterosigma akashiwo virus, HcV was more widely infectious to H. circularisquama strains that had been independently isolated in the western part of Japan, and only 5.3% of the host-virus combinations (53 host and 10 viral strains) showed resistance to viral infection. The present results are helpful in understanding the ecology of algal host-virus systems in nature.     

Diverse responses of the bivalve-killing dinoflagellate Heterocapsa circularisquama to infection by a single-stranded RNA virus

Viruses are believed to be significant pathogens for phytoplankton. Usually, they infect a single algal species, and often their infection is highly strain specific. However, the detailed molecular background of the strain specificity and its ecological significance have not been sufficiently understood. Here, we investigated the temporal changes in viral RNA accumulation and virus-induced cell lysis using a bloom-forming dinoflagellate Heterocapsa circularisquama and its single-stranded RNA virus, HcRNAV. We observed at least three host response patterns to virus inoculation: sensitive, resistant, and delayed lysis. In the sensitive response, the host cell culture was permissive for viral RNA replication and apparent cell lysis was observed; in contrast, resistant cell culture was nonpermissive for viral RNA replication and not lysed. In the delayed-lysis response, although viral RNA replication occurred, virus-induced cell lysis was faint and remarkably delayed. In addition, the number of infectious virus particles released to the culture supernatant at 12 days postinoculation was comparable to that of the sensitive strain. By further analysis, a few strains were characterized as variants of the delayed-lysis strain. These observations indicate that the response of H. circularisquama to HcRNAV infection is highly diverse.     

Spring bloom succession,grazing impact and herbivore selectivity of ciliate communities in response to winter warming

This study aimed at simulating different degrees of winter warming and at assessing its potential effects on ciliate succession and grazing-related patterns. By using indoor mesocosms filled with unfiltered water from Kiel Bight, natural light and four different temperature regimes, phytoplankton spring blooms were induced and the thermal responses of ciliates were quantified. Two distinct ciliate assemblages, a pre-spring and a spring bloom assemblage, could be detected, while their formation was strongly temperature-dependent. Both assemblages were dominated by Strobilidiids; the pre-spring bloom phase was dominated by the small Strobilidiids Lohmaniella oviformis, and the spring bloom was mainly dominated by large Strobilidiids of the genus Strobilidium. The numerical response of ciliates to increasing food concentrations showed a strong acceleration by temperature. Grazing rates of ciliates and copepods were low during the pre-spring bloom period and high during the bloom ranging from 0.06 (Δ0°C) to 0.23 day⁻¹ (Δ4°C) for ciliates and 0.09 (Δ0°C) to 1.62 day⁻¹ (Δ4°C) for copepods. During the spring bloom ciliates and copepods showed a strong dietary overlap characterized by a wide food spectrum consisting mainly of Chrysochromulina sp., diatom chains and large, single-celled diatoms. Priority programme of the German Research Foundation—contribution 4.     

Algicidal activity of the thiazolidinedione derivative TD49 against the harmful dinoflagellate Heterocapsa circularisquama in a mesocosm enclosure

To assess the algicidal effects of the thiazolidinedione derivative TD49 on the unarmored dinoflagellate Heterocapsa circularisquama and to evaluate the response of the planktonic community and the environment to this chemical, we undertook mesocosm (1,300 L) and small-scale experiments. The reduction ratio for H. circularisquama in each experiment was dependent on the concentration of TD49. At a TD49 concentration >0.4 μM, the abundance of H. circularisquama decreased by 99 % in the small-scale experiment and by 84 % in the mesocosm during the initial 2 days. At 0.2 μM TD49, the abundance of H. circularisquama decreased by up to 85 % in the small-scale experiment, whereas the abundance in the mesocosm increased, implying the absence of an algicidal effect. The decrease in planktonic organisms, including H. circularisquama, following TD49 treatment was correlated with abrupt declines in culture pH and dissolved oxygen concentration. Following addition of TD49, there was a significant increase in the abundance of diatoms and cryptophyta species, and after 8 days, the dominant species in the TD49 treatments shifted to small pennate diatoms including Cylindrotheca and Entomoneis species. The growth of some species among the zooplankton community was promoted at low TD49 concentrations (≤0.4 μM), whereas high concentrations (≥1.0 μM) had a negative effect. This study demonstrates that TD49 is an effective agent for the control for H. circularisquama blooms and that large-scale mesocosms play a crucial role in assessing the application of algicides such as TD49 in natural environments.     

Ecological dynamics of the bivalve-killing dinoflagellate Heterocapsa circularisquama and its infectious viruses in different locations of western Japan

We studied the ecological relationships between the bloom-forming dinoflagellate Heterocapsa circularisquama and its infectious viruses in field surveys conducted in western Japan. The occurrence of H. circularisquama blooms in Imari Bay during 2002 and in Ago Bay during 2002 and 2004 was accompanied by specific increase in abundance of viruses lytic to H. circularisquama. Using northern dot-blot analysis, approximately 96% of the clonal virus isolates collected in the field surveys positively reacted with a molecular probe specific for HcRNAV (H. circularisquama RNA virus); hence, viral impacts on H. circularisquama population observed in these field surveys are considered largely due to HcRNAV and/or its closely related viruses. The dynamics of type UA viruses and type CY viruses having complementary host ranges to H. circularisquama clones were different in each survey and considered to reflect fluctuations in abundance of their suitable host cells in situ. The dynamics of H. circularisquama and its viruses in Ago Bay from 2002 to 2004 suggests the concentration of HcRNAV in the sediment prior to the host's blooming season is a significant factor in determining the size and length of the H. circularisquama blooms. These results support the hypothesis that HcRNAV infection is one of the significant factors affecting the population dynamics of H. circularisquama in both quantity (biomass) and quality (clonal composition).     

Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom

Processing of the phytoplankton-derived organic sulfur compound dimethylsulfoniopropionate (DMSP) by bacteria was studied in seawater microcosms in the coastal Gulf of Mexico (Alabama). Modest phytoplankton blooms (peak chlorophyll a [Chl a] concentrations of approximately 2.5 microg liter(-1)) were induced in nutrient-enriched microcosms, while phytoplankton biomass remained low in unamended controls (Chl a concentrations of approximately 0.34 microg liter(-1)). Particulate DMSP concentrations reached 96 nM in the enriched microcosms but remained approximately 14 nM in the controls. Bacterial biomass production increased in parallel with the increase in particulate DMSP, and nutrient limitation bioassays in the initial water showed that enrichment with DMSP or glucose caused a similar stimulation of bacterial growth. Concomitantly, increased bacterial consumption rate constants of dissolved DMSP (up to 20 day(-1)) and dimethylsulfide (DMS) (up to 6.5 day(-1)) were observed. Nevertheless, higher DMSP S assimilation efficiencies and higher contribution of DMSP to bacterial S demand were found in the controls compared to the enriched microcosms. This indicated that marine bacterioplankton may rely more on DMSP as a source of S under oligotrophic conditions than under the senescence phase of phytoplankton blooms. Phylogenetic analysis of the bacterial assemblages in all microcosms showed that the DMSP-rich algal bloom favored the occurrence of various Roseobacter members, flavobacteria (Bacteroidetes phylum), and oligotrophic marine Gammaproteobacteria. Our observations suggest that the composition of the bacterial assemblage and the relative contribution of DMSP to the overall dissolved organic sulfur/organic matter pool control how efficiently bacteria assimilate DMSP S and thereby potentially divert it from DMS production.     

Copepod grazing in a summer cyanobacteria bloom in the Gulf of Finland

Blooms of the cyanobacteria Nodularia spumigena and Aphanizomenon flos-aquae dominated the phytoplankton assemblages of the western Gulf of Finland and the eastern side of the northern Baltic Sea in late July–August, 1992. The bloom overlapped the peak seasonal contributions of the dominant mesozooplankton herbivores in the region, the copepods Acartia bifilosa and Eurytemora affinis and the cladoceran Bosmina longispina maritima. Using radio-labelling techniques; the copepods were offered one of the cyanobacteria, Nodularia, as well as the 10–54 µm fraction of the natural phytoplankton assemblage. In general, incorporation rates of the labelled phytoplankton into the copepods declined with increasing contributions of the cyanobacteria. For both copepods, incorporation was inversely related to total phytoplankton biomass, whether measured as chlorophyll, total cells or cyanobacteria biomass. The very low rates for Acartia (< 0.8 µl [copepod h]^–1) indicated that this copepod was likely starving in the cyanobacteria bloom, consistent with the generally poor condition of the animal observed in the laboratory. The other major mesozooplanktor, B. longispina maritima, ingested substantially more cyanobacterial biomass than the two copepods, based on HPLC-identified cyanobacteria-specific pigment echinenone in the gut. Bloom carbon provided < 1% and < 4% of the daily rations for Acartia and Eurytemora, respectively. Total copepod demand in the cyanobacteria blooms was trivial, < 1% of bloom biomass consumed daily. These results suggest that copepod herbivory is relatively unimportant in dissipating summer cyanobacteria blooms in the Gulf of Finland.     

Successional changes in the genetic diversity of a marine bacterial assemblage during confinement

The successional changes in the genetic diversity of Mediterranean bacterioplankton subjected to confinement were studied in an experimental 300 1 seawater enclosure. Five samples were taken at different times and analyzed by polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) fingerprinting to rapidly monitor changes in the bacterial genetic diversity. DGGE analysis clearly showed variations between the samples. Three of the five samples, with different DGGE banding patterns, were further analyzed by cloning and sequencing of 16S rRNA genes. Comparative sequence analysis indicated a shift from a mixed bacterial assemblage to a community dominated by bacteria closely affiliated to a single genus, Alteromonas. Sequences obtained at the start of the experiment were affiliated with two alpha-proteobacterial and three gamma-proteobacterial lineages known from other studies of marine picoplankton. One sequence was affiliated with the Verrucomicrobiales. After 161 h of incubation two sequences represented a gamma-proteobacterial lineage also present at 0 h, but the majority of sequences clustered around that of Alteromonas macleodii. After 281 h only the dominant Alteromonas-like bacteria and bacteria distantly related to Legionella were found by cloning and sequencing. Mortality rates of bacteria indicated that grazing was the dominant mortality process when heterotrophic protozoa were abundant. Hence, changes in the genetic diversity of bacteria were partly influenced by the differential mortality of bacterial populations during the course of incubation.     

Temporal changes in the sponge holobiont during the course of infection with Aplysina Red Band Syndrome

Coral Reefs - Diseases of marine organisms, including sponges on coral reefs, are being reported with increasing frequency worldwide. Aplysina Red Band Syndrome (ARBS) occurs across the Caribbean...     

Temporal evolution and vertical stratification of Microcystis toxic potential during a first bloom event

In order to study the setup of a Microcystis bloom and the evolution of its toxic potential, we studied the temporal and vertical variations in Microcystis aeruginosa abundance, microcystins (MC) concentrations (intracellular and extracellular), and the relative proportion of potentially microcystin-producing cells (MC-producing cells) in relation to physicochemical parameters in the recently setup Moroccan reservoir “Yaacoub Al Mansour.” The Microcystis bloom appeared relatively late in the season and was associated with a low proportion of MC-producing cells in the water surface layer, probably related to non-limiting nutrient concentrations. Interestingly, the setup of the bloom leads to a vertical gradient, showing a decrease in Microcystis cell abundance inversely coupled with an increase in the proportion of MC-producing cells. Thus, this can be the result of the growth where non-MC-producing cells remain in the lighted water layer easier than MC-producing ones. Nevertheless, parameters other than light intensity may influence the toxic potential of bloom as no vertical pattern was observed concerning microcystins cellular quotas. The high microcystins concentrations measured in the deep water layer have also proved the importance of considering the deep part of aquatic ecosystem in the management of health risks associated with cyanobacterial proliferations.     

Comparative study on the toxic effects of red tide flagellates Heterocapsa circularisquama and Chattonella marina on the short-necked clam (Ruditapes philippinarum)

Heterocapsa circularisquama showed much higher toxic effects on short-necked clams than Chattonella marina. Clams exposed to H. circularisquama exhibited morphological changes concomitant with an accumulation of mucus-like substances in the gills, a profound reduction in filtration activity, and lysosomal destabilization in hemocytes. Chattonella marina was less effective than H. circularisquama, and Heterocapsa triquetra was almost harmless in all these criteria. These results suggest that H. circularisquama exerted its lethal effect on short-necked clams through gill tissue damage and subsequent induction of physiological stress.     

Changes in the ciliate assemblage along a fluvial system related to physical, chemical and geomorphological characteristics

Samples were collected monthly from the water-sediment interface at six stations along the Mincio River (northern Italy) during a 1-year study of the ciliated protozoan communities. Four stations were located upstream of the Mantua lakes in the hyporhithron fluvial zone and two stations were located in the potamon fluvial zone between the Mantua lakes and the confluence with the Po River. A total of 133 species of active trophic ciliates belonging to 76 genera were found. Community structures revealed in this data were analysed using some statistical methods (similarity index, and categorical principal component analysis (CATPCA)) and this allowed the determination of differences between stations and between ciliate communities characteristic of stations. Species typical of the ecotypes located in both rhithron and potamon fluvial zones were defined. The saprobic index and valency analysis methods were used to quantify organic input and to follow changes in saprobicity along the river. A change in the ciliate communities was observed between stations located upstream and stations located downstream of the town of Mantua. The former were composed mainly of beta-mesosaprobic species, typical of the hill zone of running waters, while in the latter increased numbers of alpha-mesosaprobic species are associated with the higher anthropogenic pressures. Our results reiterate the high sensitivity shown by ciliated protozoa as indicators of organic load in watercourses.     

Microbial community changes during a toxic cyanobacterial bloom in an alkaline Hungarian lake

The Carpathian Basin is a lowland plain located mainly in Hungary. Due to the nature of the bedrock, alluvial deposits, and a bowl shape, many lakes and ponds of the area are characterized by high alkalinity. In this study, we characterized temporal changes in eukaryal and bacterial community dynamics with high throughput sequencing and relate the changes to environmental conditions in Lake Velence located in Fejér county, Hungary. The sampled Lake Velence microbial populations (algal and bacterial) were analyzed to identify potential correlations with other community members and environmental parameters at six timepoints over 6 weeks in the Spring of 2012. Correlations between community members suggest a positive relationship between certain algal and bacterial populations (e.g. Chlamydomondaceae with Actinobacteria and Acidobacteria), while other correlations allude to changes in these relationships over time. During the study, high nitrogen availability may have favored non-nitrogen fixing cyanobacteria, such as the toxin-producing Microcystis aeruginosa, and the eutrophic effect may have been exacerbated by high phosphorus availability as well as the high calcium and magnesium content of the Carpathian Basin bedrock, potentially fostering exopolymer production and cell aggregation. Cyanobacterial bloom formation could have a negative environmental impact on other community members and potentially affect overall water quality as well as recreational activities. To our knowledge, this is the first prediction for relationships between photoautotrophic eukaryotes and bacteria from an alkaline, Hungarian lake.     

Copepod feeding in the ocean: scaling patterns,composition of their diet and the bias of estimates due to microzooplankton grazing during incubations

Here, we report insights from the compilation and analysis of data on marine calanoid copepod feeding rates in the ocean. Our study shows that food availability and body weight are major factors shaping copepod feeding rates in the field, with a relatively minor role of temperature. Although the maximal feeding rates of copepods that are observed in the field agree with the well-known 3/4 of body size scaling rule for animals, copepod feeding in the oceans is typically limited and departs from this rule. Ciliates and dinoflagellates appear to be highly relevant in the composition of copepod diets, and this represents an indirect increase in the flux of primary production that is likely to reach the upper trophic levels; this contribution is higher in the less productive systems and may help to explain accounts of proportionally higher standing stocks of copepods supported per unit of primary producer biomass in oligotrophic environments. Contrary to common belief, diatoms emerge from our dataset as small contributors to the diet of copepods, except in some very productive ecosystems. We have also evaluated the bias in the estimation of copepod grazing rates due to within-bottle trophic cascade effects caused by the removal of microheterotrophs by copepods. This release of microzooplankton grazing pressure accounts for a relevant, but moderate, increase in copepod grazing estimates (ca. 20–30%); this bias has an effect on both the carbon flux budgets through copepods and on our view of their diet composition. However, caution is recommended against the indiscriminate use of corrections because they may turn out to be overestimates of the bias. We advise that both uncorrected and corrected grazing rates should be provided in future studies, as they probably correspond to the lower and upper boundaries of the true grazing rates.