Phytoplankton blooms characterize temperate ocean margin zones in spring. We investigated the bacterioplankton response to a diatom bloom in the North Sea and observed a dynamic succession of populations at genus-level resolution. Taxonomically distinct expressions of carbohydrate-active enzymes (transporters; in particular, TonB-dependent transporters) and phosphate acquisition strategies were found, indicating that distinct populations of Bacteroidetes, Gammaproteobacteria, and Alphaproteobacteria are specialized for successive decomposition of algal-derived organic matter. Our results suggest that algal substrate availability provided a series of ecological niches in which specialized populations could bloom. This reveals how planktonic species, despite their seemingly homogeneous habitat, can evade extinction by direct competition.

A process of global importance in carbon cycling is the remineralization of algae biomass by heterotrophic bacteria, most notably during massive marine algae blooms. Such blooms can trigger secondary blooms of planktonic bacteria that consist of swift successions of distinct bacterial clades, most prominently members of the Flavobacteriia, Gammaproteobacteria and the alphaproteobacterial Roseobacter clade. We investigated such successions during spring phytoplankton blooms in the southern North Sea (German Bight) for four consecutive years. Dense sampling and high-resolution taxonomic analyses allowed the detection of recurring patterns down to the genus level. Metagenome analyses also revealed recurrent patterns at the functional level, in particular with respect to algal polysaccharide degradation genes. We, therefore, hypothesize that even though there is substantial inter-annual variation between spring phytoplankton blooms, the accompanying succession of bacterial clades is largely governed by deterministic principles such as substrate-induced forcing.DOI: http://dx.doi.org/10.7554/eLife.11888.001

Bacteroidetes are widespread in marine systems where they play a crucial role in organic matter degradation. Whole genome analysis of several strains has revealed a broad glycolytic and proteolytic potential. In this study, we used a targeted metagenomic approach to investigate the degradation capabilities of distinct Bacteroidetes clades from two contrasting regions of the North Atlantic Ocean, the Polar Biome (BPLR) and the North Atlantic Subtropical (NAST). We present here the analysis of 76 Bacteroidetes fosmids, of which 28 encode the 16S rRNA gene as phylogenetic marker, and their comparison to complete Bacteroidetes genomes. Almost all of the 16S rRNA harbouring fosmids belonged to clades that we previously identified in BPLR and NAST. The majority of sequenced fosmids could be assigned to Bacteroidetes affiliated with the class Flavobacteria. We also present novel genomic information on the classes Cytophagia and Sphingobacteria, suggesting a capability of the latter for attachment to algal surfaces. In our fosmid set we identified a larger potential for polysaccharide degradation and cell surface attachment in the phytoplankton-rich BPLR. Particularly, two flavobacterial fosmids, one affiliated with the genus Polaribacter, showed a whole armoury of enzymes that likely function in degradation of sulfated polysaccharides known to be major constituents of phytoplankton cell walls. Genes involved in protein and peptidoglycan degradation, although present in both fosmid sets, seemed to have a slight preponderance in NAST. This study provides support for the hypothesis of a distinct specialization among marine Bacteroidetes for the degradation of certain types of polymers.

The genome encodes the metabolic and functional capabilities of an organism and should be a major determinant of its ecological niche. Yet, it is unknown if the niche can be predicted directly from the genome. Here, we conduct metagenomic binning on 123 water samples spanning major environmental gradients of the Baltic Sea. The resulting 1961 metagenomeassembled genomes represent 352 species-level clusters that correspond to 1/3 of the metagenome sequences of the prokaryotic size-fraction. By using machine-learning, the placement of a genome cluster along various niche gradients (salinity level, depth, sizefraction) could be predicted based solely on its functional genes. The same approach predicted the genomes' placement in a virtual niche-space that captures the highest variation in distribution patterns. The predictions generally outperformed those inferred from phylogenetic information. Our study demonstrates a strong link between genome and ecological niche and provides a conceptual framework for predictive ecology based on genomic data.

The Baltic Sea is one of the world’s largest brackish water bodies and is characterised by pronounced physicochemical gradients where microbes are the main biogeochemical catalysts. Meta-omic methods provide rich information on the composition of, and activities within, microbial ecosystems, but are computationally heavy to perform. We here present the Baltic Sea Reference Metagenome (BARM), complete with annotated genes to facilitate further studies with much less computational effort. The assembly is constructed using 2.6 billion metagenomic reads from 81 water samples, spanning both spatial and temporal dimensions, and contains 6.8 million genes that have been annotated for function and taxonomy. The assembly is useful as a reference, facilitating taxonomic and functional annotation of additional samples by simply mapping their reads against the assembly. This capability is demonstrated by the successful mapping and annotation of 24 external samples. In addition, we present a public web interface, BalticMicrobeDB, for interactive exploratory analysis of the dataset.

The roles of individual bacterioplankton species in the re-mineralization of algal biomass are poorly understood. Evidence from molecular data had indicated that a spring diatom bloom in the German Bight of the North Sea in 2009 was followed by a rapid succession of uncultivated bacterioplankton species, including members of the genera Ulvibacter, Formosa, Polaribacter (class Flavobacteria) and Reinekea (class Gammaproteobacteria). We isolated strains from the same site during the diatom bloom in spring 2010 using dilution cultivation in an artificial seawater medium with micromolar substrate and nutrient concentrations. Flow cytometry demonstrated growth from single cells to densities of 10(4) -10(6) cells ml(-1) and a culturability of 35%. Novel Formosa, Polaribacter and Reinekea strains were isolated and had 16S rRNA gene sequence identities of > 99.8% with bacterioplankton in spring or summer 2009. Genomes of selected isolates were draft sequenced and used for read recruitment of metagenomes from bacterioplankton in 2009. Metagenome reads covered 93% of a Formosa clade B, 91% of a Reinekea and 74% of a Formosa clade A genome, applying a ≥ 94.5% nucleotide identity threshold. These novel strains represent abundant bacterioplankton species thriving on coastal phytoplankton blooms in the North Sea.

Marine Bacteroidetes have pronounced capabilities of degrading high molecular weight organic matter such as proteins and polysaccharides. Previously we reported on 76 Bacteroidetes-affiliated fosmids from the North Atlantic Ocean's boreal polar and oligotrophic subtropical provinces. Here, we report on the analysis of further 174 fosmids from the same libraries. The combined, re-assembled dataset (226 contigs; 8.8 Mbp) suggests that planktonic Bacteroidetes at the oligotrophic southern station use more peptides and bacterial and animal polysaccharides, whereas Bacteroidetes at the polar station (East-Greenland Current) use more algal and plant polysaccharides. The latter agrees with higher abundances of algae and terrigenous organic matter, including plant material, at the polar station. Results were corroborated by in-depth bioinformatic analysis of 14 polysaccharide utilisation loci from both stations, suggesting laminarin-specificity for four and specificity for sulfated xylans for two loci. In addition, one locus from the polar station supported use of non-sulfated xylans and mannans, possibly of plant origin. While peptides likely represent a prime source of carbon for Bacteroidetes in open oceans, our data suggest that as yet unstudied clades of these Bacteroidetes have a surprisingly broad capacity for polysaccharide degradation. In particular, laminarin-specific PULs seem widespread and thus must be regarded as globally important.

The degradation of diatoms is mainly catalyzed by Bacteroidetes and this process is of global relevance for the carbon cycle. In this study, a combination of catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) and fluorescent lectin binding analysis (FLBA) was used to identify and map glycoconjugates involved in the specific interactions of Bacteroidetes and diatoms, as well as detritus, at the coastal marine site Helgoland Roads (German Bight, North Sea). The study probed both the presence of lectin-specific extracellular polymeric substances (EPS) of Bacteroidetes for cell attachment and that of glycoconjugates on diatoms with respect to binding sites for Bacteroidetes. Members of the clades Polaribacter and Ulvibacter were shown to form microcolonies within aggregates for which FLBA indicated the presence of galactose containing slime. Polaribacter spp. was shown to bind specifically to the setae of the abundant diatom Chaetoceros spp., and the setae were stained with fucose-specific lectins. In contrast, Ulvibacter spp. attached to diatoms of the genus Asterionella which bound, among others, the mannose-specific lectin PSA. The newly developed CARD-FISH/FLBA protocol was limited to the glycoconjugates that persisted after the initial CARD-FISH procedure. The differential attachment of bacteroidetal clades to diatoms and their discrete staining by FLBA provided evidence for the essential role that formation and recognition of glycoconjugates play in the interaction of bacteria with phytoplankton.