Heterotrophic Nanoflagellates Growth Research Articles

Ocean acidification reduces growth and grazing impact of Antarctic heterotrophic nanoflagellates

Abstract. High-latitude oceans have been identified as particularly vulnerable to ocean acidification if anthropogenic CO2 emissions continue. Marine microbes are an essential part of the marine food web and are a critical link in biogeochemical processes in the ocean, such as the cycling of nutrients and carbon. Despite this, the response of Antarctic marine microbial communities to ocean acidification is poorly understood. We investigated the effect of increasing fCO2 on the growth of heterotrophic nanoflagellates (HNFs), nano- and picophytoplankton, and prokaryotes (heterotrophic Bacteria and Archaea) in a natural coastal Antarctic marine microbial community from Prydz Bay, East Antarctica. At CO2 levels ≥634 µatm, HNF abundance was reduced, coinciding with increased abundance of picophytoplankton and prokaryotes. This increase in picophytoplankton and prokaryote abundance was likely due to a reduction in top-down control of grazing HNFs. Nanophytoplankton abundance was elevated in the 634 µatm treatment, suggesting that moderate increases in CO2 may stimulate growth. The taxonomic and morphological differences in CO2 tolerance we observed are likely to favour dominance of microbial communities by prokaryotes, nanophytoplankton, and picophytoplankton. Such changes in predator–prey interactions with ocean acidification could have a significant effect on the food web and biogeochemistry in the Southern Ocean, intensifying organic-matter recycling in surface waters; reducing vertical carbon flux; and reducing the quality, quantity, and availability of food for higher trophic levels.

Bacterial prey food characteristics modulate community growth response of freshwater bacterivorous flagellates

AbstractDifferent bacterioplankton species represent different food quality resources for heterotrophic nanoflagellate (HNF) communities, potentially affecting HNF growth, community dynamics and carbon flow to higher trophic levels. However, our knowledge of such dynamics is still very limited. Here, we describe the results of 11 experiments with natural HNF communities from distinct seasonal phases in two freshwater habitats. The HNF communities were released from predation pressure of zooplankton and incubated with 16 distinct ecologically relevant prey bacterial strains from important Betaproteobacteria genera (Limnohabitans, Polynucleobacter, and Methylopumilus) and one Actinobacteria strain from the Luna 2 cluster. We observed remarkable prey‐ and season‐specific variability in community HNF growth parameters, i.e., doubling time, volumetric gross growth efficiency (GGE), and length of lag phase. All strains, except for the actinobacterium, supported rapid HNF population growth with an average doubling time of 10 h and GGE of 29%. Our analysis revealed that 59% of the variability in flagellate GGE data was explained by the length of lag phase after prey amendments. This indicates a considerable “adaptation time,” during which the predator communities undergo compositional shifts toward flagellate bacterivores best adapted to grow on the offered prey. Importantly, the rapid HNF growth detected on various bacteria tightly corresponds to doubling times reported for fast growing bacterioplankton groups. We propose a conceptual model explaining the tight linkages between rapid bacterial community shifts and succeeding HNF community shifts, which optimize prey utilization rates and carbon flow from various bacteria to the microbial food chain.

Prey-Specific Growth Responses of Freshwater Flagellate Communities Induced by Morphologically Distinct Bacteria from the Genus Limnohabitans.

Because their large growth potential is counterbalanced with grazing by heterotrophic nanoflagellates (HNF), bacteria of the genus Limnohabitans, which are common in many freshwater habitats, represent a valuable model for examining bacterial carbon flow to the grazer food chain. We conducted experiments with natural HNF communities taken from two distinct habitats, the meso-eutrophic Římov Reservoir and the oligo-mesotrophic Lake Cep (South Bohemia). HNF communities from each habitat at distinct seasonal phases, a late April algal bloom and a late May clear water phase, were each fed 3 Limnohabitans strains of differing cell sizes. Water samples were prefiltered (5 μm) to release natural HNF communities from zooplankton control and then amended with the Limnohabitans strains L. planktonicus II-D5 (medium sized, rod shaped), Limnohabitans sp. strain T6-5 (thin, long, curved rod), and Limnohabitans sp. strain 2KL-3 (large solenoid). Using temporal sampling and prey treatment, we determined HNF growth parameters such as doubling time, growth efficiency, and length of lag phase prior starting to exponential growth. All three Limnohabitans strains supported HNF growth but in significant prey-, site-, and season-dependent fashions. For instance, addition of the moderately large T6-5 strain yielded very rapid HNF growth with a short lag phase. In contrast, the curved morphology and larger cell size of strain 2KL-3 made this prey somewhat protected against grazing by smaller HNF, resulting in slower HNF growth and longer lag phases. These trends were particularly pronounced during the late May clear-water phase, which was dominated by smaller HNF cells. This may indicate a longer "adaptation time" for the flagellate communities toward the large prey size offered.

Differential freshwater flagellate community response to bacterial food quality with a focus on Limnohabitans bacteria

Different bacterial strains can have different value as food for heterotrophic nanoflagellates (HNF), thus modulating HNF growth and community composition. We examined the influence of prey food quality using four Limnohabitans strains, one Polynucleobacter strain and one freshwater actinobacterial strain on growth (growth rate, length of lag phase and growth efficiency) and community composition of a natural HNF community from a freshwater reservoir. Pyrosequencing of eukaryotic small subunit rRNA amplicons was used to assess time-course changes in HNF community composition. All four Limnohabitans strains and the Polynucleobacter strain yielded significant HNF community growth while the actinobacterial strain did not although it was detected in HNF food vacuoles. Notably, even within the Limnohabitans strains we found significant prey-related differences in HNF growth parameters, which could not be related only to size of the bacterial prey. Sequence data characterizing the HNF communities showed also that different bacterial prey items induced highly significant differences in community composition of flagellates. Generally, Stramenopiles dominated the communities and phylotypes closely related to Pedospumella (Chrysophyceae) were most abundant bacterivorous flagellates rapidly reacting to addition of the bacterial prey of high food quality.

Functional structure of microbial food web in the Senegal River Estuary (West Africa): impact of metazooplankton

We studied the impact of various metazooplanktonic predators (two calanoid copepods and barnacle larvae) on microbial plankton isolated from the Senegal River Estuary. Experiments performed in microcosms were based on size-class fractionation (3, 12, 20 and 60 µm size classes) of the microbial community in order to obtain different assemblages, including bacteria, heterotrophic nanoflagellates (HNF), ciliates, pico- and nanophytoplankton. Removal of bacterial predators >3 µm increased the net growth rate of heterotrophic bacteria from 0.437 day−1 in the presence of all predators (fraction <60 µm) to 0.682 day−1 (fraction <3 µm). Removal of protozoa >12 µm caused an increased net growth rate of flagellates from 0.102 day−1 (fraction <60 µm) to 0.332 day−1 (fraction <12 µm). The same results were also observed on protozoa dynamics in the presence of Temora stylifera (0.498 day−1), suggesting a trophic control of the protozoa >12 µm by this copepod, allowing an increase in HNF growth rates through indirect effect. The highest ingestion rate over 60 h of experiment was recorded for the copepod Temora (61.1 µm3 ngC−1 h−1) and the lowest value for barnacle larvae (25.6 µm3 ngC−1 h−1). An intermediate value (47.5 µm3 ngC−1 h−1) was recorded for the copepod Acartia clausi. All these ingestion rates were mainly channeled in the size classes between <3 and 15–18 µm equivalent spherical diameter (ESD) (6 and 2435 µm3, respectively), with the highest values noted between <3 and 6–9 µm classes. In the presence of Temora, the cascading effects can explain both the decreases in mean volume and in growth rate for bacteria, due to the filtration of ciliates by the zooplanktonic predator, allowing the development of the HNF. The presence of a large size class of bacteria (among the five classes identified by flow cytometry) and a high abundance of HNF suggest an efficient heterotrophic pathway within the microbial loop of this sub-saharan estuary.

Turbulence effects on cold ocean microbial communities: an enclosure study

There have been numerous studies on turbulence effects on macro- and zooplankton during the last decade, but studies on microplankton have been fewer, sometimes contradictory, and conducted largely under temperate conditions. In the present study, an enclosure experiment was carried out with natural seawater of Logy Bay, Newfoundland to determine the effects of turbulence on heterotrophic and autotrophic growth in the presence and absence of micrograzers. The experiment was conducted in February with water temperatures at 0 °C. We found no difference in bacterial growth between the static and turbulence enclosures in either the presence or absence of micrograzers. Heterotrophic nanoflagellate growth, however, was found to be significantly higher in the presence of turbulence but only when micrograzers were absent. A similar pattern was found with the small autotrophic community, determined as chlorophyll a passing through a 5-μm filter, in which growth was significantly higher with turbulence but only when micrograzers were absent. Turbulence significantly enhanced growth rates of the large autotrophic community (chlorophyll a retained by a 5-μm filter), which was largely composed of diatoms, both in the presence and absence of grazers. These results suggest that turbulence effects are small under cold ocean conditions, but increase with the size of the organism. It thus appears that turbulence could affect patterns of biogenic carbon export differentially, being dependent upon the conditions of the marine environment.

Growth and production of free-living heterotrophic nanoflagellates in a eutrophic lake - Lake Donghu, Wuhan, China

In situ growth of heterotrophic nanoflagellates (HNF) in Lake Donghu, a eutrophic shallow lake in mainland China, was studied from January 1999 to March 2000 using a modified Weisse protocol. The study results indicated that the growth rates of HNF showed pronounced seasonal variation (-0.37-1.25 d(-1)), reaching the maximum during spring to early summer. When the water temperature was higher than 25.5 degreesC, HNF growth was inversely proportional to water temperature. There was an effect by bacterial abundance and autotrophic picoplankton on HNF growth that depended on location. HNF biomass was the highest in late spring, and the HNF production ranged from -2.25 to 35.45 mg l(-1) d(-1) with mean of 3.17 mg l(-1) d(-1). When considered in the context of biomass and production data for zooplankton in Lake Donghu, it was evident that HNF contributed significantly to the total zooplankton production in Lake Donghu. These in situ studies indicate that temperature and food supply are the major determinants of HNF abundance and productivity.

Top‐down effects on pelagic heterotrophic nanoflagellates (HNF) in a large river (River Rhine): do losses to the benthos play a role?

1. The abundance, production and control of pelagic heterotrophic nanoflagellates (HNF) in the Lower River Rhine (Germany) were investigated. Field samples (live‐counting technique) were taken at least every 2 weeks at Cologne (km 685) over a period of 20 months. In addition, Lagrangian sampling was carried out 160 km downstream of Cologne (Kalkar–Grieth, km 845) over a period of 12 months. Potential HNF growth rates and loss rates caused by planktonic predators were estimated in the laboratory (size fractionation experiments) and compared with the changes in HNF‐density in a water parcel flowing downstream.2. Mean abundance (±SD) ranged from 7 ± 6 to 4890 ± 560 individuals mL–1 and was positively correlated with discharge. Heterotrophic nanoflagellates abundance increased up to 30‐fold during flood events, whereas there were only minor changes in the taxonomic composition.3. HNF growth rate ranged from 0.16 ± 0.12 to 1.98 ± 0.10 day–1. Between 0 and 95% (mean: 32%) of the gross production was lost to planktonic predators; a larger portion between 0 and 195% (mean: 64%) of the HNF gross production was lost by other means.4. There may be an important role for benthic predators in the control of pelagic HNF. First, production of HNF was high and grazing losses to planktonic predators low at times when HNF abundance was low. Secondly, high in situ loss rates (not explicable by planktonic predators), which were positively related to temperature, indicate the importance of biotic interactions. Thirdly, the dependence of HNF abundance on discharge indicated a decrease grazing intensity with rising water levels (increase in water volume/colonised river bed ratio).5. The impact of discharge on planktonic HNF mediated by the grazing impact of benthic predators was modelled, showing a good fit with the field data.

Trophic interactions between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake

Trophic interactions between the mesozooplankton and the microbial web (bacteria, protozoa) were studied in 2 in situ grazing experiments in the epilimnion and the deep chlorophyll maximum (DCM) of a mesotrophic lake. We combined the Landry-Hassett dilution technique, whereby growth and grazing rates can be determined simultaneously, with the presence or absence of mesozooplankton and additional nutrients. The epilimnion was cladoceran-dominated, and had relatively high ciliate, and low heterotrophic nanoflagellate (HNF) abundance, while the DCM was rotifer-dominated, with fewer ciliates, but higher HNF abundance. Temperature differed by 13°C (22°C in the epilimnion; 9°C in the DCM). The community differences between the epilimnion and DCM and the experimental manipulations had their greatest effects on ciliates, lesser effects on HNF, and essentially no net effect on bacteria. Bacteria growth rates and grazing losses did not differ between the epilimnion and DCM, despite the large differences in chlorophyll a and abiotic parame- ters, and were independent of nutrient addition or mesozooplankton removal. In contrast, the exper- imental manipulations produced relatively moderate changes in HNF growth rates and grazing losses in both the epilimnion and DCM. Although HNF densities were 3 times higher in the DCM than the epilimnion, epilimnetic HNF growth rates were approximately twice the rate found in the DCM. This was consistent with both higher temperature and a release from predation through indi- rect predatory effects on alternative HNF predators like ciliates. In the DCM, crustacean zooplank- ton were less abundant and therefore had smaller direct and indirect effects on the HNF, while the metazoan microzooplankton (mainly rotifers) were more important. Ciliate growth rates were lower in the epilimnion than in the DCM, but only in the epilimnion were ciliate growth rates enhanced by the addition of nutrients. The cladoceran-dominated community of the epilimnion was able to reduce ciliate growth rates to negative values, while in the rotifer-dominated DCM, ciliate growth rates were always positive along a predator density gradient. These results demonstrate that while ciliates, and to a lesser extent heterotrophic flagellates, respond quickly to changes in predator community com- position, there are so many other direct and indirect pressures on bacteria that changes in the meso- zooplankton community composition have no net effect on their adundance.

Growth and production of heterotrophic nanoflagellates in a meso-eutrophic lake

The growth of heterotrophic nanoflagellates (HNF) in mesotrophic Lake Constance was measured in situ during a 13 month period. Experiments were conducted with 10 urn pre-filtered late water incubated in diffusion chambers at 3 m water depth at the sampling location for 24 h. Growth rates were calculated from changes in cell numbers occurring during the period of incubation. Growth rates of all dominant taxa showed pronounced seasonal variation (-0.13 to 1.76 day') and were gener- ally highest in summer at high water temperatures. In situ growth rates were well below maximum growth rates known for the respective and similar species from laboratory experiments. While water temperature was a key parameter positively related to the growth of all HNF species, the effect of various potential food items was taxon specific and less clear. Bacterial abundance was equally impor- tant as temperature for growth in the small bacterivorous Spumella sp., but was insignificant for growth rates of the larger omnivorous Kathablepharis sp. In Spumella sp., 84% of the observed seasonal variation of its gTowth rate could be explained by temperature and bacterial food supply. Based on these results, a multiple linear regression equation with temperature and bacterial concen- tration as dependent variables was calculated for the growth rate of Spumella. Taxon-specific pro- duction rates were derived from growth rates and average biomass of these two species, and compared to total HNF production estimated from previously measured community growth rates and biomass in Lake Constance. Production peaks of Spumella sp. and Kathablepharis sp. alternated seasonally. Total HNF production ranged from -0.01 to 10 mg C m~3 day1. The average seasonal production varied between 1.4 and 3.5 mg C nr3 day-1 over 6 consecutive years. These small protozoa thus con- tribute a substantial amount to total zooplankton production in Lake Constance.

Community structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum

AME Aquatic Microbial Ecology Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsSpecials AME 12:49-63 (1997) - doi:10.3354/ame012049 Community structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum Simek K, Hartman P, Nedoma J, Pernthaler J, Springmann D, Vrba J, Psenner R An intensive 5 wk study was conducted to investigate the role of protists, especially heterotrophic nanoflagellates (HNF), in microbial food webs during the summer phytoplankton bloom in the epilimnion and metalimnion of the eutrophic Rímov reservoir (South Bohemia, Czech Republic). On average, protists consumed ~90% of bacterial production in both layers. The community composition of HNF and the relative importance of different HNF groups as picoplankton consumers were determined. Small HNF (<8 μm), as chrysomonads, bodonids and choanoflagellates, usually accounted for <30% of total HNF biomass but numerically dominated the community in both layers. They consumed most of (~70 to 85%) the bacterioplankton as well as autotrophic picoplankton (APP, exclusively cyanobacteria) production in the reservoir, with the rest consumed by ciliates. Both ciliates and HNF had higher clearance rates on APP than on bacteria and their grazing was likely responsible for a sharp decrease in APP abundance (from 3-4 × 105 to <2 × 103 ml-1) and a very constant size structure of bacterioplankton in which short rods in the size class of 0.4 to 0.8 μm constituted 55 to 80% of the total bacterial biomass in both layers. The proportion of HNF to total picoplankton biomass in the epilimnion indicated that the picoplankton biomass was sufficiently high to support HNF growth for most of the study. Uptake of picoplankton by less numerous, but larger, HNF (kathablepharids, Goniomonas sp., and Streptomonas sp.) was negligible, while their biomass, especially in the metalimnion, exceeded that of small HNF and the total biomass of picoplankton. This suggested that food items other than picoplankton were consumed to meet their carbon requirements. Analyzing potential bottom-up and top-down factors controlling HNF numbers and biomass, we did not find a tight relationship between HNF and the concentration of bacteria and chlorophyll. Variability of HNF abundance and biomass in the epilimnion could largely be explained by cladocerans or by pooled abundances of all potential crustacean consumers of HNF. In the metalimnion, the mean cell volume of HNF was positively linked to chlorophyll but negatively to the abundance of Cyclopidae and to the pooled abundances of Ceriodaphnia quadrangula and Diaphanosoma brachyurum. Nanoflagellates · Community structure · Picoplanktivory · Bacterial production · Food webs Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in AME Vol. 12, No. 1. Publication date: January 30, 1997 Print ISSN: 0948-3055; Online ISSN: 1616-1564 Copyright © 1997 Inter-Research.