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Onset of the spring bloom in the northwestern Mediterranean Sea: influence of environmental pulse events on the in situ hourly-scale dynamics of the phytoplankton community structure.

ABSTRACT: Most of phytoplankton influence is barely understood at the sub meso scale and daily scale because of the lack of means to simultaneously assess phytoplankton functionality, dynamics and community structure. For a few years now, it has been possible to address this objective with an automated in situ high frequency sampling strategy. In order to study the influence of environmental short-term events (nutrients, wind speed, precipitation, solar radiation, temperature, and salinity) on the onset of the phytoplankton bloom in the oligotrophic Bay of Villefranche-sur-Mer (NW Mediterranean Sea), a fully remotely controlled automated flow cytometer (CytoSense) was deployed on a solar-powered platform (EOL buoy, CNRS-Mobilis). The CytoSense carried out single-cell analyses on particles (1-800 μm in width, up to several mm in length), recording optical pulse shapes when analyzing several cm(3). Samples were taken every 2 h in the surface waters during 2 months. Up to 6 phytoplankton clusters were resolved based on their optical properties (PicoFLO, Picoeukaryotes, Nanophytoplankton, Microphytoplankton, HighSWS, HighFLO). Three main abundance pulses involving the 6 phytoplankton groups monitored indicated that the spring bloom not only depends on light and water column stability, but also on short-term events such as wind events and precipitation followed by nutrient pulses. Wind and precipitation were also determinant in the collapse of the clusters' abundances. These events occurred within a couple of days, and phytoplankton abundance reacted within days. The third abundance pulse could be considered as the spring bloom commonly observed in the area. The high frequency data-set made it possible to study the phytoplankton cell cycle based on daily cycles of forward scatter and abundance. The combination of daily cell cycle, abundance trends and environmental pulses will open the way to the study of phytoplankton short-term reactivity to environmental conditions.

SUBMITTER: Thyssen M

PROVIDER: S-EPMC4129916 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:In temperate systems, phytoplankton spring blooms deplete inorganic nutrients and are major sources of organic matter for the microbial loop. In response to phytoplankton exudates and environmental factors, heterotrophic microbial communities are highly dynamic and change their abundance and composition both on spatial and temporal scales. Yet, most of our understanding about these processes comes from laboratory model organism studies, mesocosm experiments or single temporal transects. Spatial-temporal studies examining interactions of phytoplankton blooms and bacterioplankton community composition and function, though being highly informative, are scarce. In this study, pelagic microbial community dynamics (bacteria and phytoplankton) and environmental variables were monitored during a spring bloom across the Baltic Proper (two cruises between North Germany to Gulf of Finland). To test to what extent bacterioplankton community composition relates to the spring bloom, we used next generation amplicon sequencing of the 16S rRNA gene, phytoplankton diversity analysis based on microscopy counts and population genotyping of the dominating diatom Skeletonema marinoi. Several phytoplankton bloom related and environmental variables were identified to influence bacterial community composition. Members of Bacteroidetes and Alphaproteobacteria dominated the bacterial community composition but the bacterial groups showed no apparent correlation with direct bloom related variables. The less abundant bacterial phyla Actinobacteria, Planctomycetes, and Verrucomicrobia, on the other hand, were strongly associated with phytoplankton biomass, diatom:dinoflagellate ratio, and colored dissolved organic matter (cDOM). Many bacterial operational taxonomic units (OTUs) showed high niche specificities. For example, particular Bacteroidetes OTUs were associated with two distinct genetic clusters of S. marinoi. Our study revealed the complexity of interactions of bacterial taxa with inter- and intraspecific genetic variation in phytoplankton. Overall, our findings imply that biotic and abiotic factors during spring bloom influence bacterial community dynamics in a hierarchical manner.

Project description:Annually recurring phytoplankton spring blooms are characteristic of temperate coastal shelf seas. During these blooms, environmental conditions, including nutrient availability, differ considerably from non-bloom conditions, affecting the entire ecosystem including the bacterioplankton. Accordingly, the emerging ecological niches during bloom transition are occupied by different bacterial populations, with Roseobacter RCA cluster and SAR92 clade members exhibiting high metabolic activity during bloom events. In this study, the functional response of the ambient bacterial community toward a Phaeocystis globosa bloom in the southern North Sea was studied using metaproteomic approaches. In contrast to other metaproteomic studies of marine bacterial communities, this is the first study comparing two different cell lysis and protein preparation methods [using trifluoroethanol (TFE) and in-solution digest as well as bead beating and SDS-based solubilization and in-gel digest (BB GeLC)]. In addition, two different mass spectrometric techniques (ESI-iontrap MS and MALDI-TOF MS) were used for peptide analysis. A total of 585 different proteins were identified, 296 of which were only detected using the TFE and 191 by the BB GeLC method, demonstrating the complementarity of these sample preparation methods. Furthermore, 158 proteins of the TFE cell lysis samples were exclusively detected by ESI-iontrap MS while 105 were only detected using MALDI-TOF MS, underpinning the value of using two different ionization and mass analysis methods. Notably, 12% of the detected proteins represent predicted integral membrane proteins, including the difficult to detect rhodopsin, indicating a considerable coverage of membrane proteins by this approach. This comprehensive approach verified previous metaproteomic studies of marine bacterioplankton, e.g., detection of many transport-related proteins (17% of the detected proteins). In addition, new insights into e.g., carbon and nitrogen metabolism were obtained. For instance, the C1 pathway was more prominent outside the bloom and different strategies for glucose metabolism seem to be applied under the studied conditions. Furthermore, a higher number of nitrogen assimilating proteins were present under non-bloom conditions, reflecting the competition for this limited macro nutrient under oligotrophic conditions. Overall, application of different sample preparation techniques as well as MS methods facilitated a more holistic picture of the marine bacterioplankton response to changing environmental conditions.

Project description:Phytoplankton blooms exhibit a severe impact on bacterioplankton communities as they change nutrient availabilities and other environmental factors. In the current study, the response of a bacterioplankton community to a Phaeocystis globosa spring bloom was investigated in the southern North Sea. For this purpose, water samples were taken inside and reference samples outside of an algal spring bloom. Structural changes of the bacterioplankton community were assessed by amplicon-based analysis of 16S rRNA genes and transcripts generated from environmental DNA and RNA, respectively. Several marine groups responded to bloom presence. The abundance of the Roseobacter RCA cluster and the SAR92 clade significantly increased in bloom presence in the total and active fraction of the bacterial community. Functional changes were investigated by direct sequencing of environmental DNA and mRNA. The corresponding datasets comprised more than 500 million sequences across all samples. Metatranscriptomic data sets were mapped on representative genomes of abundant marine groups present in the samples and on assembled metagenomic and metatranscriptomic datasets. Differences in gene expression profiles between non-bloom and bloom samples were recorded. The genome-wide gene expression level of Planktomarina temperata, an abundant member of the Roseobacter RCA cluster, was higher inside the bloom. Genes that were differently expressed included transposases, which showed increased expression levels inside the bloom. This might contribute to the adaptation of this organism toward environmental stresses through genome reorganization. In addition, several genes affiliated to the SAR92 clade were significantly upregulated inside the bloom including genes encoding for proteins involved in isoleucine and leucine incorporation. Obtained results provide novel insights into compositional and functional variations of marine bacterioplankton communities as response to a phytoplankton bloom.

Project description:BackgroundThe planktonic bacterial community associated with spring phytoplankton blooms in the North Sea is responsible for a large amount of carbon turnover in an environment characterised by high primary productivity. Individual clades belonging to the Gammaproteobacteria have shown similar population dynamics to Bacteroidetes species, and are thus assumed to fill competing ecological niches. Previous studies have generated large numbers of metagenome assembled genomes and metaproteomes from these environments, which can be readily mined to identify populations performing potentially important ecosystem functions. In this study we attempt to catalogue these spring bloom-associated Gammaproteobacteria, which have thus far attracted less attention than sympatric Alphaproteobacteria and Bacteroidetes.MethodsWe annotated 120 non-redundant species-representative gammaproteobacterial metagenome assembled genomes from spring bloom sampling campaigns covering the four years 2010-2012 and 2016 using a combination of Prokka and PfamScan, with further confirmation via BLAST against NCBI-NR. We also matched these gene annotations to 20 previously published metaproteomes covering those sampling periods plus the spring of 2009.ResultsMetagenome assembled genomes with clear capacity for polysaccharide degradation via dedicated clusters of carbohydrate active enzymes were among the most abundant during blooms. Many genomes lacked gene clusters with clearly identifiable predicted polysaccharide substrates, although abundantly expressed loci for the uptake of large molecules were identified in metaproteomes. While the larger biopolymers, which are the most abundant sources of reduced carbon following algal blooms, are likely the main energy source, some gammaproteobacterial clades were clearly specialised for smaller organic compounds. Their substrates range from amino acids, monosaccharides, and DMSP, to the less expected, such as terpenoids, and aromatics and biphenyls, as well as many 'unknowns'. In particular we uncover a much greater breadth of apparent methylotrophic capability than heretofore identified, present in several order level clades without cultivated representatives.ConclusionsLarge numbers of metagenome assembled genomes are today publicly available, containing a wealth of readily accessible information. Here we identified a variety of predicted metabolisms of interest, which include diverse potential heterotrophic niches of spring bloom-associated Gammaproteobacteria. Features such as those identified here could well be fertile ground for future experimental studies.

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Onset of the spring bloom in the northwestern Mediterranean Sea: influence of environmental pulse events on the in situ hourly-scale dynamics of the phytoplankton community structure.

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