Picocyanobacteria and deep-ocean fluorescent dissolved organic matter share similar optical properties

Marine chromophoric dissolved organic matter (CDOM) and its related fluorescent components (FDOM), which are widely distributed but highly photobleached in the surface ocean, are critical in regulating light attenuation in the ocean. However, the origins of marine FDOM are still under investigation. Here we show that cultured picocyanobacteria, Synechococcus and Prochlorococcus, release FDOM that closely match the typical fluorescent signals found in oceanic environments. Picocyanobacterial FDOM also shows comparable apparent fluorescent quantum yields and undergoes similar photo-degradation behaviour when compared with deep-ocean FDOM, further strengthening the similarity between them. Ultrahigh-resolution mass spectrometry (MS) and nuclear magnetic resonance spectroscopy reveal abundant nitrogen-containing compounds in Synechococcus DOM, which may originate from degradation products of the fluorescent phycobilin pigments. Given the importance of picocyanobacteria in the global carbon cycle, our results indicate that picocyanobacteria are likely to be important sources of marine autochthonous FDOM, which may accumulate in the deep ocean

Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria

Background: The picocyanobacterial genus Synechococcus occurs over wide oceanic expanses, having colonized most available niches in the photic zone. Large scale distribution patterns of the different Synechococcus clades (based on 16S rRNA gene markers) suggest the occurrence of two major lifestyles ('opportunists'/'specialists'), corresponding to two distinct broad habitats ('coastal'/'open ocean'). Yet, the genetic basis of niche partitioning is still poorly understood in this ecologically important group. Results: Here, we compare the genomes of 11 marine Synechococcus isolates, representing 10 distinct lineages. Phylogenies inferred from the core genome allowed us to refine the taxonomic relationships between clades by revealing a clear dichotomy within the main subcluster, reminiscent of the two aforementioned lifestyles. Genome size is strongly correlated with the cumulative lengths of hypervariable regions (or 'islands'). One of these, encompassing most genes encoding the light-harvesting phycobilisome rod complexes, is involved in adaptation to changes in light quality and has clearly been transferred between members of different Synechococcus lineages. Furthermore, we observed that two strains (RS9917 and WH5701) that have similar pigmentation and physiology have an unusually high number of genes in common, given their phylogenetic distance. Conclusion: We propose that while members of a given marine Synechococcus lineage may have the same broad geographical distribution, local niche occupancy is facilitated by lateral gene transfers, a process in which genomic islands play a key role as a repository for transferred genes. Our work also highlights the need for developing picocyanobacterial systematics based on genome-derived parameters combined with ecological and physiological data

Invasion of a littoral cladoceran Sida crystallina into the pelagic zone of Christine Lake, NH and its potential impact on the phytoplankton community

This study evaluated the phytoplankton community and grazing influences of the zooplankton in oligotrophic Christine Lake, NH, by assessing the body size and clearance rates of the three dominant crustaceans: Sida crystallina (0.08 individuals L-1 ), Daphnia dubia (0.11 individuals L-1 ), and Leptodiaptomus sicilis (2.11 individuals L-1 ). Sida crystallina, typically a littoral cladoceran, was abundant throughout the water column in the open water, and contributed approximately 44% of the grazing in the pelagic zone. Phytoplankton abundance was examined to assess the potential impact S. crystallina might have on the phytoplankton in Christine lake. Aphanocapsa, the dominant phytoplankton in Christine Lake (relative abundance 68.54%), is a picocyanobacterium capable of forming colonies in the presence of planktonic grazers. Its ability to out-compete other phytoplankton due to differential grazing pressure suggests the appearance of the strong grazer S. crystallina may have contributed to the dominance of cyanobacteria in this oligotrophic lake

PtrA is required for coordinate regulation of gene expression during phosphate stress in a marine Synechococcus

Previous microarray analyses have shown a key role for the two-component system PhoBR (SYNW0947, SYNW0948) in the regulation of P transport and metabolism in the marine cyanobacterium Synechococcus sp. WH8102. However, there is some evidence that another regulator, SYNW1019 (PtrA), probably under the control of PhoBR, is involved in the response to P depletion. PtrA is a member of the cAMP receptor protein transcriptional regulator family that shows homology to NtcA, the global nitrogen regulator in cyanobacteria. To define the role of this regulator, we constructed a mutant by insertional inactivation and compared the physiology of wild-type Synechcococcus sp. WH8102 with the ptrA mutant under P-replete and P-stress conditions. In response to P stress the ptrA mutant failed to upregulate phosphatase activity. Microarrays and quantitative RT-PCR indicate that a subset of the Pho regulon is controlled by PtrA, including two phosphatases, a predicted phytase and a gene of unknown function psip1 (SYNW0165), all of which are highly upregulated during P limitation. Electrophoretic mobility shift assays indicate binding of overexpressed PtrA to promoter sequences upstream of the induced genes. This work suggests a two-tiered response to P depletion in this strain, the first being PhoB-dependent induction of high-affinity PO4 transporters, and the second the PtrA-dependent induction of phosphatases for scavenging organic P. The levels of numerous other transcripts are also directly or indirectly influenced by PtrA, including those involved in cell-surface modification, metal uptake, photosynthesis, stress responses and other metabolic processes, which may indicate a wider role for PtrA in cellular regulation in marine picocyanobacteria

The Distinctive Regulation of Cyanobacterial Glutamine Synthetase

Glutamine synthetase (GS) features prominently in bacterial nitrogen assimilation as it catalyzes the entry of bioavailable nitrogen in form of ammonium into cellular metabolism. The classic example, the comprehensively characterized GS of enterobacteria, is subject to exquisite regulation at multiple levels, among them gene expression regulation to control GS abundance, as well as feedback inhibition and covalent modifications to control enzyme activity. Intriguingly, the GS of the ecologically important clade of cyanobacteria features fundamentally different regulatory systems to those of most prokaryotes. These include the interaction with small proteins, the so-called inactivating factors (IFs) that inhibit GS linearly with their abundance. In addition to this protein interaction-based regulation of GS activity, cyanobacteria use alternative elements to control the synthesis of GS and IFs at the transcriptional level. Moreover, cyanobacteria evolved unique RNA-based regulatory mechanisms such as glutamine riboswitches to tightly tune IF abundance. In this review, we aim to outline the current knowledge on the distinctive features of the cyanobacterial GS encompassing the overall control of its activity, sensing the nitrogen status, transcriptional and post-transcriptional regulation, as well as strain-specific differences.Deutsche Forschungsgemeinschaft KL 3114/2-1Ministerio de Economía y Competitividad BIO2016-75634-PFEDER BIO2016-75634-

Freshwater Picocyanobacteria and their Organic Diet:An Investigation into Organic Nitrogen Assimilation in Freshwater Picocyanobacteria

Freshwater picocyanobacteria are an essential component of our waterbodies, fulfilling a role of global primary producers in waters which are often limited or co-limited by nitrogen. However, they remain relatively poorly understood, especially in comparison to their marine relatives. Also poorly understood is the picocyanobacterial metabolism of organic sources of nitrogen. Researchhas traditionally focused on inorganic sources such as ammonium or nitrate, however it is becoming increasingly evident that organic nitrogen is bioavailable and an integral component of the freshwater nitrogen pool. In this thesis,we sequence five strains of freshwater picocyanobacteria and compare theirencoding capabilities to a common Synechococcus model cyanobacterium (Synechococcus elongatus). We increased the representation of freshwater picocyanobacteria, and found reduced encoding of nitrite-associatedassimilation genes in picocyanobacteria. Further differences in encoded antennae proteins highlight the differences between freshwater picocyanobacteria (Synechococcus spp. of the Syn/Proclade) and Synechococcus elongatus, highlighting the need for a ’true’ freshwater picocyanobacterium model organism. Utilising comparative genomic analyses we investigated the nitrogen assimilation capabilities of freshwater picocyanobacteria, comparing these to picocyanobacteria of different habitatsin addition to larger freshwater cyanobacteria. The diversity displayed among nitrogen assimilation capabilities reveals the evolutionary history of the picocyanobacteria, showcasing the environments in which these organisms evolved. These analyses revealed significant variation in the encoded aminoacid transporters between freshwater picocyanobacteria and larger freshwater cyanobacteria. With different amino acid transporters having different amino acid preferences and uptake rates, this may have implications for amino acid bioavailability. Other sources of potentially differentially bioavailable nitrogen include novel organic forms, such as chitin and glyphosate. Finally, we conduct a growth assay to determine the assimilation capabilities of amino acids as an organic nitrogen source, and explore the proteomic response to growth on selected amino acids using quantitative proteomic analysis. The growth assay revealed widespread amino acid assimilation as a sole nitrogen source for freshwater picocyanobacteria, enabling a wide N pool which may contribute to their limnetic dominance. However, proteomic analysis revealed a subtle stress response in freshwater picocyanobacteria when grown on selected amino acids, potentially due to the accumulation of metabolites. Together, the work increasesour understanding of the nitrogen assimilation capabilities of freshwater picocyanobacteria, with a focus on organic sources of nitrogen

Seasonal patterns and interannual variability of phytoplankton in Lake Stechlin

The paper presents results of detailed phytoplankton investigations in Lake Stechlin between 1994 and 2003. The analysis includes the picoplankton fraction (dominated by Cyanobium sp.) that regularly appears as a deep-layer chlorophyll maximum (DCM). Planktothrix and Aulacoseira are successful competitors against Cyanobium in the isothermal period, the consequences differ markedly due to the fact that Planktothrix is able and Aulacoseira is unable to accumulate in the DCM after the onset of thermocline. The „regular-Cyanobium” and „irregular-Planktothrix, -Aulacoseira” patterns of DCM development has a basic influence on ecosystem functioning. Lake Stechlin a pristine, oligo-mesotrophic deep lake, with an established and detailed monitoring system and thus has been an ideal reference site for studying the influence of global climate changes on plankton that may improve our predictive tools for impact assessment

Effects of the herbicide Roundup on freshwater microbial communities: a mesocosm study

The impact of the widely used herbicide glyphosate has been mainly studied in terrestrial weed control, laboratory bioassays, and field studies focusing on invertebrates, amphibians, and fishes. Despite the importance of phytoplankton and periphyton communities at the base of the aquatic food webs, fewer studies have investigated the effects of glyphosate on freshwater microbial assemblages. We assessed the effect of the commercial formulation Roundup using artificial earthen mesocosms. The herbicide was added at three doses: a control (without Roundup) and two treatments of 6 and 12 mg/L of the active ingredient (glyphosate). Estimates of the dissipation rate (k) were similar in the two treatments (half-lives of 5.77 and 7.37 d, respectively). The only two physicochemical parameters showing statistically significant differences between treatments and controls were the downward vertical spectral attenuation coefficient kd(λ), where λ is wavelength, and total phosphorus concentration (TP). At the end of the experiment, the treated mesocosms showed a significant increase in the ratio kd(490 nm)/kd(550 nm) and an eightfold increase in TP. Roundup affected the structure of phytoplankton and periphyton assemblages. Total micro- and nanophytoplankton decreased in abundance in treated mesocosms. In contrast, the abundance of picocyanobacteria increased by a factor of about 40. Primary production also increased in treated mesocosms (roughly by a factor of two). Similar patterns were observed in the periphytic assemblages, which showed an increased proportion of dead : live individuals and increased abundances of cyanobacteria (about 4.5-fold). Interestingly, the observed changes in the microbial assemblages were captured by the analysis of the pigment composition of the phytoplankton, the phytoplankton absorption spectra, and the analysis of the optical properties of the water. The observed changes in the structure of the microbial assemblages are more consistent with a direct toxicological effect of glyphosate rather than an indirect effect mediated by phosphorus enrichment.Fil: Pérez, Gonzalo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; ArgentinaFil: Torremorell, Ana María. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; ArgentinaFil: Mugni, Hernan Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Limnología ; ArgentinaFil: Rodriguez, Patricia Laura. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; ArgentinaFil: Vera, Maria Solange. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Do Nascimento, Mauro. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Allende, Luz. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Bustingorry, Jose Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; ArgentinaFil: Escaray, Francisco José. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; ArgentinaFil: Ferraro, Marcela Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; ArgentinaFil: Izaguirre, Irina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; ArgentinaFil: Pizarro, Haydee Norma. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; ArgentinaFil: Bonetto, Carlos Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Limnología ; ArgentinaFil: Morris, Donald P.. Lehigh University; Estados UnidosFil: Zagarese, Horacio Ernesto. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas ; Argentin

Allelopathic and bloom-forming picocyanobacteria in a changing world

Picocyanobacteria are extremely important organisms in the world’s oceans and freshwater ecosystems. They play an essential role in primary production and their domination in phytoplankton biomass is common in both oligotrophic and eutrophic waters. Their role is expected to become even more relevant with the effect of climate change. However, this group of photoautotrophic organisms still remains insufficiently recognized. Only a few works have focused in detail on the occurrence of massive blooms of picocyanobacteria, their toxicity and allelopathic activity. Filling the gap in our knowledge about the mechanisms involved in the proliferation of these organisms could provide a better understanding of aquatic environments. In this review, we gathered and described recent information about allelopathic activity of picocyanobacteria and occurrence of their massive blooms in many aquatic ecosystems. We also examined the relationships between climate change and representative picocyanobacterial genera from freshwater, brackish and marine ecosystems. This work emphasizes the importance of studying the smallest picoplanktonic fractions of cyanobacteria. © 2018 MDPI. All Rights reserved.Acknowledgments: We thank Sabina Jodłowska for execution photographic documentations of Synechococcus sp. strains on electron microscope. This study was supported by BMN grants, Poland, No. 538-G245-B568-17

THE BIOACCUMULATION OF CYANOTOXINS IN AQUATIC FOOD WEBS

Cyanobacteria are naturally occurring photosynthetic bacteria, ubiquitous in nature. Increases in temperature and nutrients have supported the proliferation of cyanobacterial growth globally, especially in freshwater systems. Many taxa can produce biotoxins referred to as “cyanotoxins”. While toxic cyanobacteria are a growing public health concern, little is known about the accumulation of cyanotoxins in lake food webs. This research investigates the seasonal occurrence and the potential role of toxic cyanobacteria in two lakes of contrasting water qualities and food web structures. Objectives of this study were to test the bioaccumulation of microcystins (MCs) and beta-methyl-alanine-amino acid (BMAA) in zooplankton. I further assessed the major zooplankton and phytoplankton communities using stable isotopes of carbon and nitrogen, with focus on the importance of zooplankton consumer types and diet sizes; picoplankton, nanoplankton and net plankton. The bioaccumulation of cyanotoxins in zooplankton were dependent on the trophic levels and feeding behaviors of the zooplankton, which vary by species, seasons and lakes. Cyanotoxin transfer was also dependent on the presence and composition of toxic cyanobacteria, including picocyanobacteria. Understanding the transfer of cyanotoxins to the zooplankton community have significant implications in determining the pathways and the bioaccumulation of cyanotoxins to higher trophic levels such as fish, wildlife and humans