Multiomics in the central Arctic Ocean for benchmarking biodiversity change.

Multiomics approaches need to be applied in the central Arctic Ocean to benchmark biodiversity change and to identify novel species and their genes. As part of MOSAiC, EcoOmics will therefore be essential for conservation and sustainable bioprospecting in one of the least explored ecosystems on Earth.

Nitrogen Fixation Influenced by Phosphorus and Nitrogen Availability in the Benthic Bloom-forming Cyanobacterium Hydrocoleum sp. Identified in a Temperate Marine Lagoon.

The nitrogen-fixing, non-heterocystous cyanobacterium Hydrocoleum sp. (Oscillatoriales) is a common epiphytic and benthic bloom-former in tropical and subtropical shallow water systems but shares high phylogenetic similarity with the planktonic, globally important diazotroph Trichodesmium. Multiphasic observations in this study resulted in unexpected identification of Hydrocoleum sp. in mass accumulations in a coastal lagoon in the Western temperate North Atlantic Ocean. Hydrocoleum physiology was examined in situ through measurements of N2 and CO2 fixation rates and expression of genes involved with N2 fixation, CO2 fixation, and phosphorus (P) stress. Bulk N2 fixation rates and Hydrocoleum nifH expression peaked at night and were strongly suppressed by dissolved inorganic nitrogen (DIN). The expression of high affinity phosphate transporter (pstS) and alkaline phosphatase (phoA) genes of Hydrocoleum was elevated during the night and negatively responded to phosphate amendments, as evidence that these mechanisms contribute to P acquisition during diazotrophic growth of Hydrocoleum in situ. This discovery at the edge of the previously known Hydrocoleum habitat range in the warming oceans raises intriguing questions about diazotrophic cyanobacterial adaptations and transitions on the benthic-pelagic continuum.

Copepod-Associated Gammaproteobacterial Alkaline Phosphatases in the North Atlantic Subtropical Gyre.

Planktonic organisms may provide a niche to associated bacteria in the oligotrophic ocean. Bacterial fitness strategies in association with copepods - abundant planktonic crustaceans - were examined by sampling and incubation experiments in the North Atlantic Subtropical Gyre (NASG). The bacterial metatranscriptome was dominated by Gammaproteobacteria and showed expression of complete bacterial pathways including chemotaxis, cell signaling, and alkaline phosphatase activity. Quantitative PCR and reverse transcriptase qPCR revealed the consistent presence and expression of alkaline phosphatase genes primarily by Vibrio spp. in the copepod association. Copepod-associated bacteria appear to respond to prevailing phosphorus limitation by using alkaline phosphatases to break down organophosphoesters, presumably originating from the copepods. The results suggest that the basin-wide tendency for phosphorus limitation in the North Atlantic Ocean is occurring at microscales in these nitrogen-enriched copepod microenvironments. The bacterial communities and their fitness strategies supported by associations with these abundant mesozooplankton are unique from the surrounding seawater and could have large-scale implications for biogeochemical cycling, marine food web structuring, and copepod and ecosystem health.

Dissolved organic matter stimulates N2 fixation and nifH gene expression in Trichodesmium.

Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the rule rather than the exception in marine photosynthetic plankton. Trichodesmium, a prominent diazotroph ubiquitous in the (sub)tropical oceans, is generally considered to obtain energy via autotrophy. While the ability of Trichodesmium to use dissolved organic phosphorus when deprived of inorganic phosphorus sources is well known, the extent to which this important cyanobacterium may benefit from other dissolved organic matter (DOM) resources is unknown. Here we provide evidence of carbon-, nitrogen- and phosphorus-rich DOM molecules enhancing N2 fixation rates and nifH gene expression in natural Trichodesmium colonies collected at two stations in the western tropical South Pacific. Sampling at a third station located in the oligotrophic South Pacific Gyre revealed no Trichodesmium but showed presence of UCYN-B, although no nifH expression was detected. Our results suggest that Trichodesmium behaves mixotrophically in response to certain environmental conditions, providing them with metabolic plasticity and adding up to the view that mixotrophy is widespread among marine microbes.

Copepods promote bacterial community changes in surrounding seawater through farming and nutrient enrichment.

Bacteria living in the oligotrophic open ocean have various ways to survive under the pressure of nutrient limitation. Copepods, an abundant portion of the mesozooplankton, release nutrients through excretion and sloppy feeding that can support growth of surrounding bacteria. We conducted incubation experiments in the North Atlantic Subtropical Gyre to investigate the response of bacterial communities in the presence of copepods. Bacterial community composition and abundance measurements indicate that copepods have the potential to influence the microbial communities surrounding and associating with them - their 'zoosphere', in two ways. First, copepods may attract and support the growth of copiotrophic bacteria including representatives of Vibrionaceae, Oceanospirillales and Rhodobacteraceae in waters surrounding them. Second, copepods appear to grow specific groups of bacteria in or on the copepod body, particularly Flavobacteriaceae and Pseudoalteromonadaceae, effectively 'farming' them and subsequently releasing them. These distinct mechanisms provide a new view into how copepods may shape microbial communities in the open ocean. Microbial processes in the copepod zoosphere may influence estimates of oceanic bacterial biomass and in part control bacterial community composition and distribution in seawater.

Copepod-Associated Gammaproteobacteria Respire Nitrate in the Open Ocean Surface Layers.

Microbial dissimilatory nitrate reduction to nitrite, or nitrate respiration, was detected in association with copepods in the oxygenated water column of the North Atlantic subtropical waters. These unexpected rates correspond to up to 0.09 nmol N copepod-1 d-1 and demonstrate a previously unaccounted nitrogen transformation in the oceanic pelagic surface layers. Genes and transcripts for both the periplasmic and membrane associated dissimilatory nitrate reduction pathways (Nap and Nar, respectively) were detected. The napA genes and transcripts were closely related with sequences from several clades of Vibrio sp., while the closest relatives of the narG sequences were Pseudoalteromonas spp. and Alteromonas spp., many of them representing clades only distantly related to previously described cultivated bacteria. The discovered activity demonstrates a novel Gammaproteobacterial respiratory role in copepod association, presumably providing energy for these facultatively anaerobic bacteria, while supporting a reductive path of nitrogen in the oxygenated water column of the open ocean.

Seasonal variation in the copepod gut microbiome in the subtropical North Atlantic Ocean.

Characterisation of marine copepod gut microbiome composition and its variability provides information on function of marine food webs, biogeochemical cycles and copepod health. Copepod gut microbiomes were investigated quarterly over two years at the Bermuda Atlantic Time-series Station in the North Atlantic Subtropical Gyre, while assessing seasonal shifts in stable and transient communities. Microbial communities were analysed using amplicon sequencing targeting the bacterial 16S rRNA V3-V4 region and the cyanobacterial ntcA gene. Persistent bacterial groups belonging to Firmicutes, Bacteroidetes and Actinobacteria were present in the copepod guts throughout the year, and showed synchronous changes, suggesting a link to variability in copepod nutritional content. The gut communities were separate from those in the seawater, suggesting the copepod gut hosts long-term, specialized communities. Major temporal variations in the gut communities during the early winter and spring, specifically a high relative abundance of Synechococcus (up to 65%), were attributed to bacterioplankton shifts in the water column, and copepod grazing on these picoplanktonic cyanobacteria. The presence of obligate and facultative anaerobes, including Clostridiales year round, suggests that anaerobic bacterial processes are common in these dynamic microhabitats in the oligotrophic open ocean.

Microbial diversity associated with copepods in the North Atlantic subtropical gyre.

Patchiness of marine microbial communities has an important influence on microbial activities in the ocean, particularly in the oligotrophic open ocean where bioavailable nutrients are otherwise scarce. Such spatial heterogeneity is present in associations with dead and living particles, including zooplankton. The microbial community composition of mesozooplankton was investigated from the Sargasso Sea using 16S rRNA amplicon pyrosequencing. Zooplankton microbiomes were studied on the copepods Undinula vulgaris, Pleuromamma spp., Sapphirina metalina, Pseudocalanus spp. and Tigriopus sp., and an amphipod, Phrosina semilunata. The overall richness was lower in the zooplankton than in the seawater, and zooplankton-specific bacterial communities were distinct from the communities in seawater. Gammaproteobacteria dominated in all zooplankton studied, with Vibrio spp. highly represented. Firmicutes were detected in all copepods, providing evidence for anaerobic conditions present on the copepods. Bacterial groups known to grow on concentrated organic substrates or to prevent biofouling were highly represented in association with copepods, suggesting they benefit from copepod-derived nutrients or carbon. The described copepod microbiome has similarities to communities previously described in coastal copepods, suggesting some aspects of the copepod microbiome are not habitat specific. The communities are distinct of that in seawater, demonstrating significant microbial patchiness in association with marine zooplankton in the oligotrophic open ocean.