Regime shift in microalgal dynamics: Impact of water level changes on planktonic and benthic algal biomass.

Whole-lake microalgal biomass surveys were carried out in Lake Balaton to investigate the seasonal, spatial, and temporal changes of benthic algae, as well as to identify the drivers of the phytobenthos. Phytobenthos was controlled mainly by light: the highest benthic algal biomass was in the shallow littoral region characterized by large grain size (sand) with good light availability but lower nutrient content in the sediment. During the investigated period, phytoplankton biomass showed a significant decrease in almost the entire lake. At the same time, the biomass of benthic algae increased significantly in the eastern areas, increasing the contribution of total lake microalgae biomass (from 20 % to 27 %). Benthic algal biomass increase can be explained by the better light supply, owing to the artificially maintained high water level which greatly mitigates water mixing. The decrease in planktonic algal biomass could be attributed to increased zooplankton grazing, which is otherwise negatively affected by mixing. As a result of the high water level, the trophic structure of the lake has been rearranged in recent decades with a shift from the planktonic life form to the benthic one while the nutrient supply has largely remained unchanged.

Where the Little Ones Play the Main Role-Picophytoplankton Predominance in the Soda and Hypersaline Lakes of the Carpathian Basin.

The extreme environmental conditions of the diverse saline inland waters (soda lakes and pans, hypersaline lakes and ponds) of the Carpathian Basin are an advantage for picophytoplankton. The abundance of picophytoplankton in these waters can be up to several orders of magnitude higher than that in freshwater shallow lakes, but differences are also found within different saline water types: higher picophytoplankton abundances were observed in hypersaline lakes compared to humic soda lakes, and their highest numbers were detected in turbid soda lakes. Moreover, their contribution to phytoplankton biomass is higher than that in shallow freshwater lakes with similar trophic states. Based on long-term data, their ratio within the phytoplankton increased with turbidity in the case of turbid soda lakes, while, in hypersaline lakes, their proportion increased with salinity. Picocyanobacteria were only detected with high abundance (>106−107 cells/mL) in turbid soda lakes, while picoeukaryotes occurred in high numbers in both turbid and hypersaline lakes. Despite the extreme conditions of the lakes, the diversity of picophytoplankton is remarkable, with the dominance of non-marine Synechococcus/Cyanobium, Choricystis, Chloroparva and uncultured trebouxiophycean green algae in the soda lakes, and marine Synechococcus and Picochlorum in the hypersaline lakes.

Dense macrophyte cover has significant structural and functional influence on planktonic microbial communities leading to bacterial success.

We intend to assess how macrophyte cover affects planktonic microbial communities by changing the physical and chemical environment, and how macrophyte-derived DOC affects the balance between autotrophy and heterotrophy/chemoorganotrophy in a shallow lake. The structure and production of phytoplankton and bacterioplankton in the open water of a large shallow lake and in the littoral zone were compared at two sampling stations with different macrophyte cover. According to the obtained results, uncoupling between bacterioplankton and phytoplankton was observed due to the high content of organic carbon of emergent macrophyte origin. While phytoplankton were regulated by TSS, bacterioplankton (in both heterotrophic and photoheterotrophic forms) were determined by dissolved organic carbon. As a result of these processes, the littoral and pelagic zones in the lake are completely separated from each other. In open water the autotrophic processes dominated, but at the sampling stations inside the reed belt, the metabolic processes shifted in the direction of chemoorganotrophy. Our results suggest that increase of macrophyte cover in shallow water bodies will increase the significance of microbe-based carbon pathways and weakens the efficiency of carbon transport from primary producers to higher trophic levels through the planktonic food chain.

Photomorphogenesis in the Picocyanobacterium Cyanobium gracile Includes Increased Phycobilisome Abundance Under Blue Light, Phycobilisome Decoupling Under Near Far-Red Light, and Wavelength-Specific Photoprotective Strategies.

Photomorphogenesis is a process by which photosynthetic organisms perceive external light parameters, including light quality (color), and adjust cellular metabolism, growth rates and other parameters, in order to survive in a changing light environment. In this study we comprehensively explored the light color acclimation of Cyanobium gracile, a common cyanobacterium in turbid freshwater shallow lakes, using nine different monochromatic growth lights covering the whole visible spectrum from 435 to 687 nm. According to incident light wavelength, C. gracile cells performed great plasticity in terms of pigment composition, antenna size, and photosystem stoichiometry, to optimize their photosynthetic performance and to redox poise their intersystem electron transport chain. In spite of such compensatory strategies, C. gracile, like other cyanobacteria, uses blue and near far-red light less efficiently than orange or red light, which involves moderate growth rates, reduced cell volumes and lower electron transport rates. Unfavorable light conditions, where neither chlorophyll nor phycobilisomes absorb light sufficiently, are compensated by an enhanced antenna size. Increasing the wavelength of the growth light is accompanied by increasing photosystem II to photosystem I ratios, which involve better light utilization in the red spectral region. This is surprisingly accompanied by a partial excitonic antenna decoupling, which was the highest in the cells grown under 687 nm light. So far, a similar phenomenon is known to be induced only by strong light; here we demonstrate that under certain physiological conditions such decoupling is also possible to be induced by weak light. This suggests that suboptimal photosynthetic performance of the near far-red light grown C. gracile cells is due to a solid redox- and/or signal-imbalance, which leads to the activation of this short-term light acclimation process. Using a variety of photo-biophysical methods, we also demonstrate that under blue wavelengths, excessive light is quenched through orange carotenoid protein mediated non-photochemical quenching, whereas under orange/red wavelengths state transitions are involved in photoprotection.

Grazing pressure-induced shift in planktonic bacterial communities with the dominance of acIII-A1 actinobacterial lineage in soda pans.

Astatic soda pans of the Pannonian Steppe are unique environments with respect to their multiple extreme physical and chemical characteristics (high daily water temperature fluctuation, high turbidity, alkaline pH, salinity, polyhumic organic carbon concentration, hypertrophic state and special ionic composition). However, little is known about the seasonal dynamics of the bacterial communities inhabiting these lakes and the role of environmental factors that have the main impact on their structure. Therefore, two soda pans were sampled monthly between April 2013 and July 2014 to reveal changes in the planktonic community. By late spring in both years, a sudden shift in the community structure was observed, the previous algae-associated bacterial communities had collapsed, resulting the highest ratio of Actinobacteria within the bacterioplankton (89%, with the dominance of acIII-A1 lineage) ever reported in the literature. Before these peaks, an extremely high abundance (> 10,000 individuum l-1) of microcrustaceans (Moina brachiata and Arctodiaptomus spinosus) was observed. OTU-based statistical approaches showed that in addition to algal blooms and water-level fluctuations, zooplankton densities had the strongest effect on the composition of bacterial communities. In these extreme environments, this implies a surprisingly strong, community-shaping top-down role of microcrustacean grazers.

Prokaryotic community composition in a great shallow soda lake covered by large reed stands (Neusiedler See/Lake Ferto) as revealed by cultivation- and DNA-based analyses.

Little is known about the detailed community composition of heterotrophic bacterioplankton in macrophyte-dominated littoral systems, where a considerable amount of dissolved organic carbon originates from aquatic macrophytes instead of phytoplankton. The aim of the present study was to reveal the effect of macrophytes on the microbial community and to elucidate their role in a macrophyte-dominated shallow soda lake, which can be characterised by a mosaic of open waters and reed marsh. Therefore, 16S rRNA gene amplicon sequencing, the most probable number method, cultivation of bacterial strains, EcoPlate and cultivation-based substrate utilisation techniques were applied. Differences in the structures of microbial communities were detected between the water and the sediment samples and between vegetated and unvegetated water samples. Planktonic bacterial communities of an inner pond and a reed-covered area showed significant similarities to each other. Woesearchaeia was the dominant archaeal taxon in the water samples, while Bathyarchaeia, 'Marine Benthic Group D' and 'DHVEG-1' were abundant in the sediment samples. The most probable number of heterotrophic bacteria was lower in the open water than in the reed-associated areas. The vast majority (83%) of the isolated bacterial strains from the water samples of the reed-covered area were able to grow on a medium containing reed extract as the sole source of carbon.

Photoautotrophic picoplankton - a review on their occurrence, role and diversity in Lake Balaton.

Occurrence of the smallest phototrophic microorganisms (photoautotrophic picoplankton, APP) in Lake Balaton was discovered in the early 1980s. This triggered a series of systematic studies on APP and resulted in the setting of a unique long-term picoplankton dataset. In this review, we intend to summarize the obtained results and to give a new insight on APP ecology and diversity in Lake Balaton. According to the results, APP dynamics depends on trophic state, temperature, nutrient, and light availability, as well as grazing pressure. APP abundance in Lake Balaton decreased to a low level (1-2 × 105 cells mL-1) as a consequence of decreasing nutrient supply (oligotrophication) during the past more than two decades, and followed a characteristic seasonal dynamics with higher abundance values from spring to autumn than in winter. Concomitantly, however, the APP contribution to both phytoplankton biomass and primary production increased (up to 70% and 40-50%, respectively) during oligotrophication. Regarding annual pattern, picocyanobacteria are dominant from spring to autumn, while in winter, picoeukaryotes are the most abundant, most likely due to the different light and temperature optima of these groups. Within picocyanobacteria, single cells and microcolonies were both observed with mid-summer dominance of the latter which correlated well with the density of cladocerans. Community-level chromatic adaptation (i.e., dominance of phycoerythrin- or phycocyanin-rich forms) of planktonic picocyanobacteria was also found as a function of underwater light quality. Sequence analysis studies of APP in Lake Balaton revealed that both picocyanobacteria and picoeukaryotes represent a diverse and dynamic community consisting several freshwater genotypes (picocyanobacteria: Synechococcus, Cyanobium; picoeukaryotes: Choricystis, Stichococcus, Mychonastes, Nannochloris, and Nannochloropsis).

Aerobic anoxygenic phototrophs are highly abundant in hypertrophic and polyhumic waters.

Aerobic anoxygenic phototrophs (AAPs) are a group of photoheterotrophic bacteria common in natural waters. Here, AAP abundance and contribution to total bacterial abundance and biomass were investigated to test whether the trophic status of a lake or content of coloured dissolved organic matter (CDOM) play a role in determining AAP distribution and abundance in shallow inland lakes, with special focus on hypertrophic and polyhumic waters. Twenty-six different shallow lakes in Hungary were monitored. AAP abundance and biomass were determined by epifluorescence microscopy. The lakes exhibit a broad range of CDOM (2-7000 mg Pt L-1) and phytoplankton biomass (2-1200 µg L-1 chlorophyll a concentration). Very high AAP abundance (up to 3 × 107 cells mL-1) was observed in polyhumic and hypertrophic shallow lakes. AAP abundance was influenced by phytoplankton biomass and CDOM content, and these effects were interrelated. As determined, 40 µg L-1 chlorophyll a and 52 mg Pt L-1 CDOM are threshold levels above which these effects have a synergistic relationship. Hence, the observed high AAP abundance in some soda pans is a consequence of combined hypertrophy and high CDOM content. AAP contribution was influenced by total suspended solids (TSS) content: the success of AAP cells could be explained by high TSS levels, which might be explained by the decrease of their selective grazing control.

Dual bloom of green algae and purple bacteria in an extremely shallow soda pan.

In April 2014, dual bloom of green algae and purple bacteria occurred in a shallow, alkaline soda pan (Kiskunság National Park, Hungary). The water was only 5 cm deep, in which an upper green layer was clearly separated from a near-sediment purple one. Based on microscopy and DNA-based identification, the upper was inhabited by a dense population of the planktonic green alga, Oocystis submarina Lagerheim, while the deeper layer was formed by purple, bacteriochlorophyll-containing bacteria, predominated by Thiorhodospira and Rhodobaca. Additional bacterial taxa with a presumed capability of anoxygenic phototrophic growth belonged to the genera Loktanella and Porphyrobacter. Comparing the bacterial community of the purple layer with a former blooming event in a nearby soda pan, similar functional but different taxonomic composition was revealed. Members from many dominant bacterial groups were successfully cultivated including potentially new species, which could be the result of the application of newly designed media.

Differences in planktonic microbial communities associated with three types of macrophyte stands in a shallow lake.

Little is known about how various substances from living and decomposing aquatic macrophytes affect the horizontal patterns of planktonic bacterial communities. Study sites were located within Lake Kolon, which is a freshwater marsh and can be characterised by open-water sites and small ponds with different macrovegetation (Phragmites australis, Nymphea alba and Utricularia vulgaris). Our aim was to reveal the impact of these macrophytes on the composition of the planktonic microbial communities using comparative analysis of environmental parameters, microscopy and pyrosequencing data. Bacterial 16S rRNA gene sequences were dominated by members of phyla Proteobacteria (36%-72%), Bacteroidetes (12%-33%) and Actinobacteria (5%-26%), but in the anoxic sample the ratio of Chlorobi (54%) was also remarkable. In the phytoplankton community, Cryptomonas sp., Dinobryon divergens, Euglena acus and chrysoflagellates had the highest proportion. Despite the similarities in most of the measured environmental parameters, the inner ponds had different bacterial and algal communities, suggesting that the presence and quality of macrophytes directly and indirectly controlled the composition of microbial plankton.

Soda pans of the Pannonian steppe harbor unique bacterial communities adapted to multiple extreme conditions.

Soda pans of the Pannonian steppe are unique environments regarding their physical and chemical characteristics: shallowness, high turbidity, intermittent character, alkaline pH, polyhumic organic carbon concentration, hypertrophic condition, moderately high salinity, sodium and carbonate ion dominance. The pans are highly productive environments with picophytoplankton predominance. Little is known about the planktonic bacterial communities inhabiting these aquatic habitats; therefore, amplicon sequencing and shotgun metagenomics were applied to reveal their composition and functional properties. Results showed a taxonomically complex bacterial community which was distinct from other soda lakes regarding its composition, e.g. the dominance of class Alphaproteobacteria was observed within phylum Proteobacteria. The shotgun metagenomic analysis revealed several functional gene components related to the harsh and at the same time hypertrophic environmental conditions, e.g. proteins involved in stress response, transport and hydrolase systems targeting phytoplankton-derived organic matter. This is the first detailed report on the indigenous planktonic bacterial communities coping with the multiple extreme conditions present in the unique soda pans of the Pannonian steppe.

Unusual behaviour of phototrophic picoplankton in turbid waters.

Autotrophic picoplankton (APP) abundance and contribution to phytoplankton biomass was studied in Hungarian shallow lakes to test the effect of inorganic turbidity determining the size distribution of the phytoplankton. The studied lakes displayed wide turbidity (TSS: 4-2250 mg l-1) and phytoplankton biomass (chlorophyll a: 1-460 µg l-1) range, as well as APP abundance (0 and 100 million cells ml-1) and contribution (0-100%) to total phytoplankton biomass. Inorganic turbidity had a significant effect on the abundance and contribution of APP, resulting in higher values compared to other freshwater lakes with the same phytoplankton biomass. Our analysis has provided empirical evidence for a switching point (50 mg l-1 inorganic turbidity), above which turbidity is the key factor causing APP predominance regardless of phytoplankton biomass in shallow turbid lakes. Our results have shown that turbid shallow lakes are unique waters, where the formerly and widely accepted model (decreasing APP contribution with increasing phytoplankton biomass) is not applicable. We hypothesize that this unusual behaviour of APP in turbid waters is a result of either diminished underwater light intensity or a reduced grazing pressure due to high inorganic turbidity.

Picophytoplankton predominance in hypersaline lakes (Transylvanian Basin, Romania).

The occurrence and importance of photoautotrophic picoplankton (PPP, cells with a diameter <2 µm) was studied along a trophic and salinity gradient in hypersaline lakes of the Transylvanian Basin (Romania). The studied lakes were found to be rich in PPP, with abundances (maximum 7.6 × 10(6) cells mL(-1)) higher than in freshwater and marine environments of similar trophic conditions. The contribution of PPP to the total phytoplankton biovolume did not decrease with increasing trophic state as it was generally found in other aquatic environments. Regardless of the trophic conditions, the contribution of PPP could reach 90-100 % in these hypersaline lakes. We hypothesized that the PPP predominance might be the result of the low grazing pressure, since heterotrophic nanoflagellates (the main grazers of PPP) were absent in the studied samples. There were significant differences in community composition among the lakes along the salinity gradient. CyPPP predominated in less saline waters (mainly below 5 %), while EuPPP were present along the entire salinity range (up to 18.7 %), dominating the phytoplankton between 3 and 13 % salinity. Above 13 % salinity, the phytoplankton was composed mainly of Dunaliella species.

Unique picoeukaryotic algal community under multiple environmental stress conditions in a shallow, alkaline pan.

Winter phytoplankton communities in the shallow alkaline pans of Hungary are frequently dominated by picoeukaryotes, sometimes in particularly high abundance. In winter 2012, the ice-covered alkaline Zab-szék pan was found to be extraordinarily rich in picoeukaryotic green algae (42-82 × 10(6) cells ml(-1)) despite the simultaneous presence of multiple stressors (low temperature and light intensity with high pH and salinity). The maximum photosynthetic rate of the picoeukaryote community was 1.4 µg C µg chlorophyll a (-1) h(-1) at 125 µmol m(-2) s(-1). The assimilation rates compared with the available light intensity measured on the field show that the community was considerably light-limited. Estimated areal primary production was 180 mg C m(-2) d(-1). On the basis of the 18S rRNA gene analysis (cloning and DGGE), the community was phylogenetically heterogeneous with several previously undescribed chlorophyte lineages, which indicates the ability of picoeukaryotic communities to maintain high genetic diversity under extreme conditions.

Planktonic bacterial community composition of an extremely shallow soda pond during a phytoplankton bloom revealed by cultivation and molecular cloning.

Böddi-szék is one of the shallow soda ponds located in the Kiskunság National Park, Hungary. In June 2008, immediately prior to drying out, an extensive algal bloom dominated by a green alga (Oocystis submarina Lagerheim) was observed in the extremely saline and alkaline water of the pond. The aim of the present study was to reveal the phylogenetic diversity of the bacterial communities inhabiting the water of Böddi-szék during the blooming event. Using two different selective media, altogether 110 aerobic bacterial strains were cultivated. According to the sequence analysis of the 16S rRNA gene, most of the strains belonged to alkaliphilic or alkalitolerant and moderately halophilic species of the genera Bacillus and Gracilibacillus (Firmicutes), Algoriphagus and Aquiflexum (Bacteroidetes), Alkalimonas and Halomonas (Gammaproteobacteria). Other strains were closely related to alkaliphilic and phototrophic purple non-sulfur bacteria of the genera Erythrobacter and Rhodobaca (Alphaproteobacteria). Analysis of the 16S rRNA gene-based clone library indicated that most of the total of 157 clone sequences affiliated with the anoxic phototrophic bacterial genera of Rhodobaca and Rhodobacter (Alphaproteobacteria), Ectothiorhodospira (Gammaproteobacteria) and Heliorestis (Firmicutes). Phylotypes related to the phylum Bacteroidetes formed the second most abundant group. Clones related to the mainly anaerobic and alkaliphilic bacterial genera of Anoxynatronum (Firmicutes), Spirochaeta (Spirochaetes) and Desulfonatronum (Deltaproteobacteria) were also abundant. Further clone sequences showed less than 95 % similarity values to cultivated species of the phyla Actinobacteria, Cyanobacteria, Deinococcus-Thermus, Fibrobacteres, Gemmatimonadetes and Lentisphaerae.

First record of picophytoplankton diversity in Central European hypersaline lakes.

Our survey has revealed that the phytoplankton in the anthropo-hypersaline lakes of the Transylvanian Basin (Romania) was often dominated by photoautotrophic picoplankton (PPP, cells with a diameter <2 µm). Therefore, the aim of this study was to identify PPP members both in the summer and the winter communities using molecular biological techniques, denaturing gradient gel electrophoresis (DGGE) and sequence analysis. The applied PCR-DGGE methods were highly specific to cyanobacteria and green algae. A total of 11 different plankton taxa were identified that were related to several distant taxonomic groups. PPP were represented by a simple community and consisted of two major genotypes, one from the green algal species Picochlorum oklahomense and the other related to marine Synechococcus isolates (Cyanobacteria). These marine PPP species were recorded for the first time in inland saline lakes from Europe. Besides picoplankton, several additional marine taxa (e.g. cryptophytes and haptophytes) were detected among the nanoplankton species. The presence of the identified marine and hypersaline species could be explained by wind, precipitation or waterfowl transfer; however, this latter could have smaller importance.