Response of Microbial Communities to Changing Climate Conditions During Summer Cyanobacterial Blooms in the Baltic Sea

Frequencies and biomass of Baltic Sea cyanobacterial blooms are expected to be higher in future climate conditions, but also of longer duration as a result of increased sea surface temperature. Concurrently, climate predictions indicate a reduced salinity in the Baltic Sea. These climate-driven changes are expected to alter not solely the phytoplankton community but also the role of microbial communities for nutrient remineralization. Here, we present the response of summer plankton communities (filamentous cyanobacteria, picocyanobacteria, and heterotrophic bacteria) to the interplay of increasing temperature (from 16 to 18°C and 20°C) and reduced salinity (from salinity 6.9 to 5.9) in the Baltic Proper (NW Gotland Sea) using a microcosm approach. Warmer temperatures led to an earlier peak of cyanobacterial biomass, while yields were reduced. These conditions caused a decrease of nitrogen-fixers (Dolichospermum sp.) biomass, while non nitrogen-fixers (Pseudanabaena sp.) increased. Salinity reduction did not affect cyanobacterial growth nor community composition. Among heterotrophic bacteria, Actinobacteria showed preference for high temperature, while Gammaproteobacteria thrived at in situ temperature. Heterotrophic bacteria community changed drastically at lower salinity and resembled communities at high temperature. Picocyanobacteria and heterotrophic bacterial biomass had a pronounced increase associated with the decay of filamentous cyanobacteria. This suggests that shifts in community composition of heterotrophic bacteria are influenced both directly by abiotic factors (temperature and salinity) and potentially indirectly by cyanobacteria. Our findings suggest that at warmer temperature, lower yield of photosynthetic cyanobacteria combined with lower proportion of nitrogen-fixers in the community could result in lower carbon export to the marine food web with consequences for the decomposer community of heterotrophic bacteria

Consistency in microbiomes in cultures of Alexandrium species isolated from brackish and marine waters

Phytoplankton and bacteria interactions have a significant role in aquatic ecosystem functioning. Associations can range from mutualistic to parasitic, shaping biogeochemical cycles and having a direct influence on phytoplankton growth. How variations in phenotype and sampling location, affect the phytoplankton microbiome is largely unknown. A high-resolution characterization of the bacterial community in cultures of the dinoflagellate Alexandrium was performed on strains isolated from different geographical locations and at varying anthropogenic impact levels. Microbiomes of Baltic Sea Alexandrium ostenfeldii isolates were dominated by Betaproteobacteria and were consistent over phenotypic and genotypic Alexandrium strain variation, resulting in identification of an A. ostenfeldii core microbiome. Comparisons with in situ bacterial communities showed that taxa found in this A. ostenfeldii core were specifically associated to dinoflagellate dynamics in the Baltic Sea. Microbiomes of Alexandrium tamarense and minutum, isolated from the Mediterranean Sea, differed from those of A. ostenfeldii in bacterial diversity and composition but displayed high consistency, and a core set of bacterial taxa was identified. This indicates that Alexandrium isolates with diverse phenotypes host predictable, species-specific, core microbiomes reflecting the abiotic conditions from which they were isolated. These findings enable in-depth studies of potential interactions occurring between Alexandrium and specific bacterial taxa

Baltic Sea phytoplankton in a changing environment

Future climate scenarios in the Baltic Sea project increasing sea surface temperature, as well as increasing precipitation and river runoff resulting in decreased salinity. These changes can severely impact the dynamics and function of brackish water communities, specifically phytoplankton. Phytoplankton are a significant source of organic matter to other trophic levels, and some species can be toxic. Their response to future climate conditions is of great relevance for the health of humans and aquatic ecosystems. The aim of this thesis was to assess the potential for climate-induced changes, such as decreasing salinity, to affect phytoplankton dynamics, physiology and chemical profiles in the Baltic Sea.      Phytoplankton successional patterns in the Baltic Proper consist of a spring bloom where diatoms and dinoflagellates co-occur and a summer bloom dominated by filamentous/colonial cyanobacteria. The consensus is that future warmer conditions will promote filamentous/colonial cyanobacteria blooms. This thesis shows that phytoplankton biomass in the spring bloom was lower in years with milder winters compared with cold winters. This suggests that in terms of annual carbon export to higher trophic levels, loss of biomass from the spring bloom is unlikely to be compensated by summer cyanobacteria. High frequency sampling of phytoplankton performed in this thesis revealed a strong relationship between the dynamics of pico- and filamentous cyanobacteria. Large genetic diversity was found in cyanobacterial populations with high niche differentiation among the same species. At community level, high temperature and low salinity were the main factors shaping the summer cyanobacterial composition. These conditions may promote the predominance of opportunistic filamentous cyanobacteria, e.g. Nodularia spumigena. This species produces various bioactive compounds, including non-ribosomal peptides such as the hepatotoxin nodularin. In this work, N. spumigena subpopulations evolved different physiological strategies, including chemical profiles, to cope with salinity stress. This high phenotypic plasticity ensures survival in future climate conditions. Under salinity stress, some subpopulations displayed shorter filaments as a trade-off. This indicates that the future freshening of the Baltic Sea may promote grazing on filamentous cyanobacteria and modify carbon flows in the ecosystem. In this thesis, Baltic N. spumigena chemotypes and genotypes grouped into two main clusters without influence of geographical origin. Thus, chemical profiling can be used to explore conspecific diversity in closely genetically related N. spumigena subpopulations.      Overall, this thesis has significantly expanded the knowledge on phytoplankton community and population responses to short- and long-term environmental changes, relevant to project the impacts of future climate conditions in the Baltic Sea

Chemical and Genetic Diversity of Nodularia spumigena from the Baltic Sea

Nodularia spumigena is a toxic, filamentous cyanobacterium occurring in brackish waters worldwide, yet forms extensive recurrent blooms in the Baltic Sea. N. spumigena produces several classes of non-ribosomal peptides (NRPs) that are active against several key metabolic enzymes. Previously, strains from geographically distant regions showed distinct NRP metabolic profiles. In this work, conspecific diversity in N. spumigena was studied using chemical and genetic approaches. NRP profiles were determined in 25 N. spumigena strains isolated in different years and from different locations in the Baltic Sea using liquid chromatography-tandem mass spectrometry (LC-MS/MS). Genetic diversity was assessed by targeting the phycocyanin intergenic spacer and flanking regions (cpcBA-IGS). Overall, 14 spumigins, 5 aeruginosins, 2 pseudaeruginosins, 2 nodularins, 36 anabaenopeptins, and one new cyanopeptolin-like peptide were identified among the strains. Seven anabaenopeptins were new structures; one cyanopeptolin-like peptide was discovered in N. spumigena for the first time. Based on NRP profiles and cpcBA-IGS sequences, the strains were grouped into two main clusters without apparent influence of year and location, indicating persistent presence of these two subpopulations in the Baltic Sea. This study is a major step in using chemical profiling to explore conspecific diversity with a higher resolution than with a sole genetic approach

Chemical and Genetic Diversity of Nodularia spumigena from the Baltic Sea

Nodularia spumigena is a toxic, filamentous cyanobacterium occurring in brackish waters worldwide, yet forms extensive recurrent blooms in the Baltic Sea. N. spumigena produces several classes of non-ribosomal peptides (NRPs) that are active against several key metabolic enzymes. Previously, strains from geographically distant regions showed distinct NRP metabolic profiles. In this work, conspecific diversity in N. spumigena was studied using chemical and genetic approaches. NRP profiles were determined in 25 N. spumigena strains isolated in different years and from different locations in the Baltic Sea using liquid chromatography-tandem mass spectrometry (LC-MS/MS). Genetic diversity was assessed by targeting the phycocyanin intergenic spacer and flanking regions (cpcBA-IGS). Overall, 14 spumigins, 5 aeruginosins, 2 pseudaeruginosins, 2 nodularins, 36 anabaenopeptins, and one new cyanopeptolin-like peptide were identified among the strains. Seven anabaenopeptins were new structures; one cyanopeptolin-like peptide was discovered in N. spumigena for the first time. Based on NRP profiles and cpcBA-IGS sequences, the strains were grouped into two main clusters without apparent influence of year and location, indicating persistent presence of these two subpopulations in the Baltic Sea. This study is a major step in using chemical profiling to explore conspecific diversity with a higher resolution than with a sole genetic approach.EcoChang

Data_Sheet_1_Response of Microbial Communities to Changing Climate Conditions During Summer Cyanobacterial Blooms in the Baltic Sea.docx

<p>Frequencies and biomass of Baltic Sea cyanobacterial blooms are expected to be higher in future climate conditions, but also of longer duration as a result of increased sea surface temperature. Concurrently, climate predictions indicate a reduced salinity in the Baltic Sea. These climate-driven changes are expected to alter not solely the phytoplankton community but also the role of microbial communities for nutrient remineralization. Here, we present the response of summer plankton communities (filamentous cyanobacteria, picocyanobacteria, and heterotrophic bacteria) to the interplay of increasing temperature (from 16 to 18°C and 20°C) and reduced salinity (from salinity 6.9 to 5.9) in the Baltic Proper (NW Gotland Sea) using a microcosm approach. Warmer temperatures led to an earlier peak of cyanobacterial biomass, while yields were reduced. These conditions caused a decrease of nitrogen-fixers (Dolichospermum sp.) biomass, while non nitrogen-fixers (Pseudanabaena sp.) increased. Salinity reduction did not affect cyanobacterial growth nor community composition. Among heterotrophic bacteria, Actinobacteria showed preference for high temperature, while Gammaproteobacteria thrived at in situ temperature. Heterotrophic bacteria community changed drastically at lower salinity and resembled communities at high temperature. Picocyanobacteria and heterotrophic bacterial biomass had a pronounced increase associated with the decay of filamentous cyanobacteria. This suggests that shifts in community composition of heterotrophic bacteria are influenced both directly by abiotic factors (temperature and salinity) and potentially indirectly by cyanobacteria. Our findings suggest that at warmer temperature, lower yield of photosynthetic cyanobacteria combined with lower proportion of nitrogen-fixers in the community could result in lower carbon export to the marine food web with consequences for the decomposer community of heterotrophic bacteria.</p

Interannual variability of phyto-bacterioplankton biomass and production in coastal and offshore waters of the Baltic Sea

The microbial part of the pelagic food web is seldom characterized in models despite its major contribution to biogeochemical cycles. In the Baltic Sea, spatial and temporal high frequency sampling over three years revealed changes in heterotrophic bacteria and phytoplankton coupling (biomass and production) related to hydrographic properties of the ecosystem. Phyto- and bacterioplankton were bottom-up driven in both coastal and offshore areas. Cold winter temperature was essential for phytoplankton to conform to the successional sequence in temperate waters. In terms of annual carbon production, the loss of the spring bloom (diatoms and dinoflagellates) after mild winters tended not to be compensated for by other taxa, not even summer cyanobacteria. These results improve our ability to project Baltic Sea ecosystem response to short- and long-term environmental changes.Supplement: 3 Special Issue: SI</p

Physical barriers and environmental gradients cause spatial and temporal genetic differentiation of an extensive algal bloom

Aim: To test if a phytoplankton bloom is panmictic, or whether geographical and environmental factors cause spatial and temporal genetic structure. Location: Baltic Sea. Method: During four cruises, we isolated clonal strains of the diatom Skeletonema marinoi from 9 to 10 stations along a 1132 km transect and analysed the genetic structure using eight microsatellites. Using F-statistics and Bayesian clustering analysis we determined if samples were significantly differentiated. A seascape approach was applied to examine correlations between gene flow and oceanographic connectivity, and combined partial Mantel test and RDA based variation partitioning to investigate associations with environmental gradients. Results: The bloom was initiated during the second half of March in the southern and the northern- parts of the transect, and later propagated offshore. By mid-April the bloom declined in the south, whereas high phytoplankton biomass was recorded northward. We found two significantly differentiated populations along the transect. Genotypes were significantly isolated by distance and by the south-north salinity gradient, which illustrated that the effects of distance and environment were confounded. The gene flow among the sampled stations was significantly correlated with oceanographic connectivity. The depletion of silica during the progression of the bloom was related to a temporal population genetic shift. Main conclusions: A phytoplankton bloom may propagate as a continuous cascade and yet be genetically structured over both spatial and temporal scales. The Baltic Sea spring bloom displayed strong spatial structure driven by oceanographic connectivity and geographical distance, which was enhanced by the pronounced salinity gradient. Temporal transition of conditions important for growth may induce genetic shifts and different phenotypic strategies, which serve to maintain the bloom over longer periods