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Toward the poles, life on land is increasingly dominated by microorganisms, yet the evolutionary origin of polar microbiomes remains poorly understood. Here, we use metabarcoding of Arctic, sub-Antarctic, and Antarctic lacustrine benthic microbial communities to test the hypothesis that high-latitude microbiomes are recruited from a globally dispersing species pool through environmental selection. We demonstrate that taxonomic overlap between the regions is limited within most phyla, even at higher-order taxonomic levels, with unique deep-branching phylogenetic clades being present in each region. We show that local and regional taxon richness and net diversification rate of regionally restricted taxa differ substantially between polar regions in both microeukaryotic and bacterial biota. This suggests that long-term evolutionary divergence resulting from low interhemispheric dispersal and diversification in isolation has been a prominent process shaping present-day polar lake microbiomes. Our findings illuminate the distinctive biogeography of polar lake ecosystems and underscore that conservation efforts should include their unique microbiota.
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Lagos , Microbiota , Filogenia , Evolución Biológica , Regiones AntárticasRESUMEN
The melting of the Greenland Ice Sheet is accelerating, with glaciers shifting from marine to land termination and potential consequences for fjord ecosystems downstream. Monthly samples in 2016 in two fjords in southwest Greenland show that subglacial discharge from marine-terminating glaciers sustains high phytoplankton productivity that is dominated by diatoms and grazed by larger mesozooplankton throughout summer. In contrast, melting of land-terminating glaciers results in a fjord ecosystem dominated by bacteria, picophytoplankton and smaller zooplankton, which has only one-third of the annual productivity and half the CO2 uptake compared to the fjord downstream from marine-terminating glaciers.
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We studied how changing human impacts affected phytoplankton dynamics in the freshwater and brackish tidal reaches of the Zeeschelde estuary (Belgium) between 2002 and 2018. Until the early 2000s, the Zeeschelde was heavily polluted due to high wastewater discharges. By 2008, water quality had improved, resulting in lower nutrient concentrations and higher oxygen levels. Since 2009, however, increased dredging activities resulted in altered hydrodynamics and increased suspended sediment concentration. The combined effects of these environmental changes were reflected in three marked transitions in phytoplankton community composition. Assemblages were dominated by Thalassiosirales and green algae (especially Scenedesmaceae) until 2003. The period 2003-2011 was characterized by the wax and wane of the centric diatoms Actinocyclus and Aulacoseira, while in the period 2012-2018 Thalassiosirales and Cyanobacteria became dominant, the latter mainly imported from the tributaries. Phytoplankton biomass increased sharply in 2003, after which there was a gradual decline until 2018. By 2018, the timing of the growing season had advanced with about one month compared to the start of the study, probably as a consequence of climate warming and intensified zooplankton grazing pressure. Our study shows that de-eutrophication (during the 2000s) and morphological interventions in the estuary (in the 2010s) were dominant drivers of phytoplankton dynamics but that the main shifts in community composition were triggered by extreme weather events, suggesting significant resistance of autochthonous communities to gradual changes in the environment.
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Diatomeas , Clima Extremo , Humanos , Fitoplancton , Estuarios , Bélgica , Hidrodinámica , Biomasa , EutrofizaciónRESUMEN
It is generally recognised that interactions between microalgae and bacteria play an important role in the functioning of marine ecosystems. In this context, increasing attention is paid to the processes that shape microalga-associated microbiomes. In recent years, conflicting evidence has been reported with respect to the relative importance of selective vs neutral processes in the assembly process. Whereas some studies report strong selection imposed by the host, others propose a more neutral, lottery-like assembly model according to which the chance of bacteria becoming part of the microbiome is proportional to their abundance in the environment and not driven by the selectional pressure created by the host. In the present study, we investigated to what degree selective vs neutral assembly processes constrain taxonomic, phylogenetic and functional variation within and between microbiomes associated with 69 isolates belonging to the Cylindrotheca closterium benthic marine diatom complex. The diatom cultures were initiated from non-axenic clonal isolates from different marine environments and geographic locations, and were then reared in a common garden (lab) environment. An important environmental imprint, likely due to in situ lottery dynamics, was apparent in the diatom microbiomes. However, microbiome assembly was also phylogenetically and functionally constrained through selective filtering related to the host microhabitat. Randomised microbiome assembly simulations revealed evidence for phylogenetic overdispersion in the observed microbiomes, reflecting an important role in the assembly process for competition between bacteria on the one hand and predominantly genetically driven differences between the hosts on the other hand. Our study thus shows that even between closely related diatom strains, host selection affects microbiome assembly, superimposing the predominantly stochastically driven recruitment process.
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The properties of incident light play a crucial role in the mating process of diatoms, a group of ecologically important microalgae. While species-specific requirements for light intensity and photoperiod have been observed in several diatom species, little is known about the light spectrum that allows sexual reproduction. Here, we study the effects of spectral properties and light intensity on the initiation and progression of sexual reproduction in the model benthic diatom Seminavis robusta. We found that distinct stages of the mating process have different requirements for light. Vigorous mating pair formation occurred under a broad range of light intensities, ranging from 10 to 81 µE m-2 s-1, while gametogenesis and subsequent stages were strongly affected by moderate light intensities of 27 µE m-2 s-1 and up. In addition, light of blue or blue-green wavelengths was required for the formation of mating pairs. Combining flow cytometric analysis with expression profiling of the diatom-specific cyclin dsCyc2 suggests that progression through a blue light-dependent checkpoint in the G1 cell cycle phase is essential for induction of sexual reproduction. Taken together, we expand the current model of mating in benthic pennate diatoms, which relies on the interplay between light, cell cycle and sex pheromone signaling.
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Diatomeas/fisiología , Diatomeas/efectos de la radiación , Puntos de Control del Ciclo Celular/efectos de la radiación , Diatomeas/genética , Diatomeas/metabolismo , Luz , Fotoperiodo , Reproducción , Atractivos Sexuales/metabolismoRESUMEN
Despite evidence for microbial endemism, an understanding of the impact of geological and paleoclimate events on the evolution of regional protist communities remains elusive. Here, we provide insights into the biogeographical history of Antarctic freshwater diatoms, using lacustrine fossils from mid-Miocene and Quaternary Antarctica, and dovetail this dataset with a global inventory of modern freshwater diatom communities. We reveal the existence of a diverse mid-Miocene diatom flora bearing similarities with several former Gondwanan landmasses. Miocene cooling and Plio-Pleistocene glaciations triggered multiple extinction waves, resulting in the selective depauperation of this flora. Although extinction dominated, in situ speciation and new colonizations ultimately shaped the species-poor, yet highly adapted and largely endemic, modern Antarctic diatom flora. Our results provide a more holistic view on the scale of biodiversity turnover in Neogene and Pleistocene Antarctica than the fragmentary perspective offered by macrofossils and underscore the sensitivity of lacustrine microbiota to large-scale climate perturbations.
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Diatoms, an evolutionarily successful group of microalgae, display high levels of intraspecific genetic variability in natural populations. However, the contribution of various mechanisms generating such diversity is unknown. Here we estimated the genetic micro-diversity within a natural diatom population and mapped the genomic changes arising within clonally propagated diatom cell cultures. Through quantification of haplotype diversity by next-generation sequencing and amplicon re-sequencing of selected loci, we documented a rapid accumulation of multiple haplotypes accompanied by the appearance of novel protein variants in cell cultures initiated from a single founder cell. Comparison of the genomic changes between mother and daughter cells revealed copy number variation and copy-neutral loss of heterozygosity leading to the fixation of alleles within individual daughter cells. The loss of heterozygosity can be accomplished by recombination between homologous chromosomes. To test this hypothesis, we established an endogenous readout system and estimated that the frequency of interhomolog mitotic recombination was under standard growth conditions 4.2 events per 100 cell divisions. This frequency is increased under environmental stress conditions, including treatment with hydrogen peroxide and cadmium. These data demonstrate that copy number variation and mitotic recombination between homologous chromosomes underlie clonal variability in diatom populations. We discuss the potential adaptive evolutionary benefits of the plastic response in the interhomolog mitotic recombination rate, and we propose that this may have contributed to the ecological success of diatoms.
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Diatomeas , Alelos , División Celular , Cromosomas , Variaciones en el Número de Copia de ADN , Diatomeas/genéticaRESUMEN
The efficiency of microalgal biomass production is a determining factor for the economic competitiveness of microalgae-based industries. N-acetylcysteine (NAC) and pluronic block polymers are two compounds of interest as novel culture media constituents because of their respective protective properties against oxidative stress and shear-stress-induced cell damage. Here we quantify the effect of NAC and two pluronic (F127 and F68) culture media additives upon the culture productivity of six marine microalgal species of relevance to the aquaculture industry (four diatoms-Chaetoceros calcitrans, Chaetoceros muelleri, Skeletonema costatum, and Thalassiosira pseudonana; two haptophytes-Tisochrysis lutea and Pavlova salina). Algal culture performance in response to the addition of NAC and pluronic, singly or combined, is dosage- and species-dependent. Combined NAC and pluronic F127 algal culture media additives resulted in specific growth rate increases of 38%, 16%, and 24% for C. calcitrans, C. muelleri, and P. salina, respectively. Enhanced culture productivity for strains belonging to the genus Chaetoceros was paired with an ~27% increase in stationary-phase cell density. For some of the species examined, culture media enrichments with NAC and pluronic resulted in increased omega-3-fatty acid content of the algal biomass. Larval development (i.e., growth and survival) of the Pacific oyster (Crassostrea gigas) was not changed when fed a mixture of microalgae grown in NAC- and F127-supplemented culture medium. Based upon these results, we propose that culture media enrichment with NAC and pluronic F127 is an effective and easily adopted approach to increase algal productivity and enhance the nutritional quality of marine microalgal strains commonly cultured for live-feed applications in aquaculture. KEY POINTS: ⢠Single and combined NAC and pluronic F127 culture media supplementation significantly enhanced the productivity of Chaetoceros calcitrans and Chaetoceros muelleri cultures. ⢠Culture media enrichments with NAC and F127 can increase omega-3-fatty acid content of algal biomass. ⢠Microalgae grown in NAC- and pluronic F127-supplemented culture media are suitable for live-feed applications.
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Microalgas , Acetilcisteína , Biomasa , Medios de Cultivo , Ácidos Grasos , Poloxámero , PolímerosRESUMEN
Sexual reproduction is a fundamental phase in the life cycle of most diatoms. Despite its role as a source of genetic variation, it is rarely reported in natural circumstances and its molecular foundations remain largely unknown. Here, we integrate independent transcriptomic datasets to prioritize genes responding to sex inducing pheromones (SIPs) in the pennate diatom Seminavis robusta. We observe marked gene expression changes associated with SIP treatment in both mating types, including an inhibition of S phase progression, chloroplast division, mitosis, and cell wall formation. Meanwhile, meiotic genes are upregulated in response to SIP, including a sexually induced diatom specific cyclin. Our data further suggest an important role for reactive oxygen species, energy metabolism, and cGMP signaling during the early stages of sexual reproduction. In addition, we identify several genes with a mating type specific response to SIP, and link their expression pattern with physiological specialization, such as the production of the attraction pheromone diproline in mating type - (MT-) and mate-searching behavior in mating type + (MT+). Combined, our results provide a model for early sexual reproduction in pennate diatoms and significantly expand the suite of target genes to detect sexual reproduction events in natural diatom populations.
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Diatomeas , Atractivos Sexuales , Diatomeas/genética , Feromonas , Reproducción , TranscriptomaRESUMEN
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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Benthic diatoms are the main primary producers in shallow freshwater and coastal environments, fulfilling important ecological functions such as nutrient cycling and sediment stabilization. However, little is known about their evolutionary adaptations to these highly structured but heterogeneous environments. Here, we report a reference genome for the marine biofilm-forming diatom Seminavis robusta, showing that gene family expansions are responsible for a quarter of all 36,254 protein-coding genes. Tandem duplications play a key role in extending the repertoire of specific gene functions, including light and oxygen sensing, which are probably central for its adaptation to benthic habitats. Genes differentially expressed during interactions with bacteria are strongly conserved in other benthic diatoms while many species-specific genes are strongly upregulated during sexual reproduction. Combined with re-sequencing data from 48 strains, our results offer insights into the genetic diversity and gene functions in benthic diatoms.
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Adaptación Fisiológica/genética , Diatomeas/genética , Ecosistema , Evolución Molecular , Genoma/genética , Diatomeas/clasificación , Diatomeas/metabolismo , Agua Dulce , Tamaño del Genoma , Genómica/métodos , Polimorfismo de Nucleótido Simple , Agua de Mar , Especificidad de la Especie , Transcriptoma/genéticaRESUMEN
Soil micro-organisms drive the global carbon and nutrient cycles that underlie essential ecosystem functions. Yet, we are only beginning to grasp the drivers of terrestrial microbial diversity and biogeography, which presents a substantial barrier to understanding community dynamics and ecosystem functioning. This is especially true for soil protists, which despite their functional significance have received comparatively less interest than their bacterial counterparts. Here, we investigate the diversification of Pinnularia borealis, a rare biosphere soil diatom species complex, using a global sampling of >800 strains. We document unprecedented high levels of species-diversity, reflecting a global radiation since the Eocene/Oligocene global cooling. Our analyses suggest diversification was largely driven by colonization of novel geographic areas and subsequent evolution in isolation. These results illuminate our understanding of how protist diversity, biogeographical patterns, and members of the rare biosphere are generated, and suggest allopatric speciation to be a powerful mechanism for diversification of micro-organisms.
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Biodiversidad , Diatomeas/crecimiento & desarrollo , Ecosistema , Microbiología del Suelo , Bacterias/clasificación , Bacterias/genética , Bacterias/crecimiento & desarrollo , Diatomeas/clasificación , Diatomeas/genética , Evolución Molecular , Geografía , Filogenia , Análisis de Secuencia de ADN , Especificidad de la EspecieRESUMEN
In the last decades, the North Sea has undergone intense environmental changes which have led to regime shifts that affected all trophic levels. Since the 1970s, both increases and decreases in phytoplankton biomass and production have been reported from different parts of the North Sea. Such conflicting observations may be partly caused by methodological differences, but also reflect regional differences related to bathymetry, hydrodynamics, climate, riverine and Atlantic influence. The Belgian part of the North Sea (BPNS) is a hydrodynamically and bathymetrically complex area under strong human influence, which has been characterized by eutrophication (up to the 1980s) and de-eutrophication (1990s onwards), and pronounced long-term changes in turbidity and water temperature. We used a newly recovered and standardized historic dataset, the Belgian Phytoplankton Database (Nohe et al., 2018), to compare the biomass, composition and seasonality of diatom and dinoflagellate assemblages, two key components of the plankton in the BPNS, between the 1970s and 2000s. Diatoms, especially large-sized taxa, showed an increase from late winter to summer, resulting in a more intense and extended growing season in the 2000s. Dinoflagellates increased year-round but especially in summer. Both diatom and dinoflagellate blooms showed a clear shift towards an earlier bloom start. In addition, while in the 1970s distinct seasonal community types were present, a striking seasonal homogenization in community structure had occurred by the 2000s. Finally, we observed a pronounced increase in the abundance of harmful diatom and dinoflagellate genera. The observed changes are most likely due to an increase in sea surface temperature and water transparency, and changes in nutrient loads and ratios. Our study underscores the importance of recovering previously inaccessible historic data as they can offer unprecedented insights into long-term change in marine ecosystems, which are essential for properly evaluating the impact of human activities on these ecosystems.
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Diatomeas , Dinoflagelados , Bélgica , Biomasa , Eutrofización , Humanos , Mar del Norte , Fitoplancton , Estaciones del AñoRESUMEN
Four Gram-negative, aerobic, rod-shaped and yellow-orange pigmented bacteria (R-46770, R-48165T, R-50232 and R-50233) were isolated from intertidal sediment and water of the Westerschelde estuary between 2006 and 2012. Analysis of their 16S rRNA gene sequences revealed that the four strains form a separate cluster between validly described type strains of the genus Leeuwenhoekiella. DNA-DNA reassociation values of two representative strains (i.e. R-48165T and R-50232) of the new group with type strains of Leeuwenhoekiella species ranged from 18.7 to 56.6â%. A comparative genome analysis of the two strains and the type strains confirmed average nucleotide identity values from 75.6 to 94.4 %. The G+C contents of the genomic DNA of strains R-48165T and R-50232 were 37.80 and 37.83âmol%, respectively. The predominant cellular fatty acids of the four novel strains were summed feature 3 (i.e. C16â:â1ω7c and/or iso-C15â:â0 2-OH), iso-C15â:â0, iso-C15â:â1 G and iso-C17â:â0 3-OH. The four new Leeuwenhoekiella-like strains grew with 0.5-12â% (w/v) NaCl, at pH 5.5-9.0 and displayed optimum growth between 20 and 30 °C. Based on the results of phenotypic, genomic, phylogenetic and chemotaxonomic analyses, the four new strains represent a novel species of the genus Leeuwenhoekiella for which the name Leeuwenhoekiella aestuarii sp. nov. is proposed. The type strain is LMG 30908T (=R-48165T=CECT 9775T=DSM 107866T). Genome analysis of type strains of the genus Leeuwenhoekiella revealed a large number of glycosyl hydrolases, peptidases and carboxyl esterases per Mb, whereas the number of transporters per Mb was low compared to other bacteria. This confirmed the environmental role of Leeuwenhoekiella species as (bio)polymer degraders, with a specialization on degrading proteins and high molecular weight compounds. Additionally, the presence of a large number of genes involved in gliding motility and surface adhesion, and large numbers of glycosyl transferases per Mb confirmed the importance of these features for Leeuwenhoekiella species.
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Flavobacteriaceae/clasificación , Sedimentos Geológicos/microbiología , Filogenia , Agua de Mar/microbiología , Técnicas de Tipificación Bacteriana , Composición de Base , ADN Bacteriano/genética , Estuarios , Ácidos Grasos/química , Flavobacteriaceae/aislamiento & purificación , Países Bajos , Pigmentación , ARN Ribosómico 16S/genética , Análisis de Secuencia de ADNRESUMEN
While different microalgae tend to be associated with different bacteria, it remains unclear whether such specific associations are beneficial for the microalgae. We assessed the impact of bacterial isolates, derived from various marine benthic diatoms, on the growth of several strains belonging to the Cylindrotheca closterium diatom species complex. We first tested the effect of 35 different bacterial isolates on the growth of a single C. closterium strain, and then evaluated the impact of 8 of these isolates on the growth of 6 C. closterium strains and 1 Cylindrotheca fusiformis strain. Surprisingly, most interactions were neutral to antagonistic. The interactions were highly specific, with diatom growth in the presence of specific bacteria differing between Cylindrotheca strains and species, and closely related bacteria eliciting contrasting diatom growth responses. These differences could be related to the origin of the bacterial isolates, as only isolates from foreign diatom hosts significantly reduced diatom growth, implying coadaptation between different Cylindrotheca strains and their associated bacteria. Interestingly, the antagonistic effect of a Marinobacter strain was alleviated by the presence of a microbial inoculum that was native to the diatom host, suggesting that coadapted bacteria might also benefit their host indirectly by preventing the establishment of harmful bacteria.
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Fenómenos Fisiológicos Bacterianos , Diatomeas/microbiología , Bacterias/aislamiento & purificación , Diatomeas/crecimiento & desarrollo , Especificidad del HuéspedRESUMEN
Coastal waters are expected to undergo severe warming in the coming decades. Very little is known about how diatoms, the dominant primary producers in these habitats, will cope with these changes. We investigated the thermal niche of Cylindrotheca closterium, a widespread benthic marine diatom, using 24 strains collected over a wide latitudinal gradient. A multi-marker phylogeny in combination with a species delimitation approach shows that C. closterium represents a (pseudo)cryptic species complex, and this is reflected in distinct growth response patterns in terms of optimum growth temperature, maximum growth rate, and thermal niche width. Strains from the same clade displayed a similar thermal response, suggesting niche conservation between closely related strains. Due to their lower maximum growth rate and smaller thermal niche width, we expect the polar species to be particularly sensitive to warming, and, in the absence of adaptation, to be replaced with species from lower latitudes.
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Benthic diatoms are dominant primary producers in intertidal mudflats and constitute a major source of organic carbon to consumers and decomposers residing within these ecosystems. They typically form biofilms whose species richness, community composition and productivity can vary in response to environmental drivers and their interactions with other organisms (e.g., grazers). Here, we investigated whether bacteria can affect diatom community composition and vice versa, and how this could influence the biodiversity-productivity relation. Using axenic experimental communities with three common benthic diatoms (Cylindrotheca closterium, Navicula phyllepta, and Seminavis robusta), we observed an increase in algal biomass production in diatom co-cultures in comparison to monocultures. The presence of bacteria decreased the productivity of diatom monocultures while bacteria did not seem to affect the overall productivity of diatoms grown in co-cultures. The effect of bacteria on diatom growth, however, appeared to be species-specific, resulting in compositional shifts when different diatom species were grown together. The effect of the diatoms on the bacteria also proved to be species-specific as each diatom species developed a bacterial community that differed in its composition. Together, our results suggest that interactions between bacteria and diatoms residing in mudflats are a key factor in the structuring of the benthic microbial community composition and the overall functioning of that community.
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Global downwelling plane irradiance is a necessary variable to normalize water-leaving radiance measurements, reducing the magnitude and spectral variabilities introduced by the incident light field. As a result, the normalized measurements, known as remote sensing reflectance, have higher correlation with the inherent optical properties of the water body and so to the composition of optically active water components. For in situ measurements, the global downwelling plane irradiance can be estimated from the exitant radiance of sintered polytetrafluoroethylene plaques or other diffuse reflectance standards. This allows use of a single spectrometer to measure all necessary variables to estimate the remote sensing reflectance, reducing cost in acquisition and maintenance of instrumentation. However, despite being in use for more than 30 years, the uncertainty associated with the method has been only partially evaluated. In this study, we use a suite of sky radiance distributions for 24 atmospheres and nine solar zenith angles in combination with full bidirectional reflectance distribution function determinations of white and gray plaques to evaluate the uncertainties. The isolated and interactive effects of bidirectional reflectance distribution, shadowing, and tilt error sources are evaluated. We find that under the best-performing geometries of each plaque, and with appropriate estimation functions, average standard uncertainty ranges from 1% to 6.5%. The simulated errors are found to explain both previous empirical uncertainty estimates and new data collected during this study. Those errors are of the same magnitude as uncertainties of plane irradiance sensors (e.g., cosine collectors) and overlap with uncertainty requirements for different uses of in situ data, which supports the continued use of the plaque method in hydrologic optics research and monitoring. Recommendations are provided to improve the quality of measurements and assure that uncertainties will be in the range of those calculated here.
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Marine bacteria contribute substantially to nutrient cycling in the oceans and can engage in close interactions with microalgae. Many microalgae harbor characteristic satellite bacteria, many of which participate in N-acyl homoserine lactone (AHL) mediated quorum sensing. In the diffusion-controlled phycosphere, AHLs can reach high local concentrations, with some of them transforming into tetramic acids, compounds with a broad bioactivity. We tested a representative AHL, N-(3-oxododecanoyl) homoserine lactone, and its tetramic acid rearrangement product on the diatom Phaeodactylum tricornutum. While cell growth and photosynthetic efficiency of photosystem II were barely affected by the AHL, exposure to its tetramic acid rearrangement product had a negative effect on photosynthetic efficiency and led to growth inhibition and cell death in the long term, with a minimum inhibitory concentration between 20 and 50 µΜ. These results strengthen the view that AHLs may play an important role in shaping the outcome of microalgae-bacteria interactions.
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4-Butirolactona/análogos & derivados , Diatomeas/efectos de los fármacos , Fotosíntesis/efectos de los fármacos , Pirrolidinonas/farmacología , 4-Butirolactona/química , 4-Butirolactona/farmacología , Diatomeas/crecimiento & desarrollo , Diatomeas/fisiologíaRESUMEN
The Belgian Phytoplankton Database (BPD) is a comprehensive data collection comprising quantitative phytoplankton cell counts from multiple research projects conducted since 1968. The collection is focused on the Belgian part of the North Sea, but also includes data from the French and the Dutch part of the North Sea. The database includes almost 300 unique sampling locations and more than 3,000 sampling events resulting in more than 86,000 phytoplankton cell count records. The dataset covers two periods: 1968 to 1978 and 1994 to 2010. The BPD can be accessed online and provides high quality phytoplankton count data. The species taxonomy is updated, and the count values are quality checked and standardized. Important metadata like sampling date, sampling location, sampling depth and methodology is provided and standardized. Additionally, associated abiotic data and biovolume values are available. The dataset allows to conduct analyses of long-term temporal and spatial trends in phytoplankton community structure in the southern part of the North Sea, including changes in phytoplankton phenology and seasonality.