Methylphosphonate-driven methane formation and its link to primary production in the oligotrophic North Atlantic.

Methylphosphonate is an organic phosphorus compound used by microorganisms when phosphate, a key nutrient limiting growth in most marine surface waters, becomes unavailable. Microbial methylphosphonate use can result in the formation of methane, a potent greenhouse gas, in oxic waters where methane production is traditionally unexpected. The extent and controlling factors of such aerobic methane formation remain underexplored. Here, we show high potential net rates of methylphosphonate-driven methane formation (median 0.4 nmol methane L-1 d-1) in the upper water column of the western tropical North Atlantic. The rates are repressed but still quantifiable in the presence of in-situ or added phosphate, suggesting that some methylphosphonate-driven methane formation persists in phosphate-replete waters. The genetic potential for methylphosphonate utilisation is present in and transcribed by key photo- and heterotrophic microbial taxa, such as Pelagibacterales, SAR116, and Trichodesmium. While the large cyanobacterial nitrogen-fixers dominate in the surface layer, phosphonate utilisation by Alphaproteobacteria appears to become more important in deeper depths. We estimate that at our study site, a substantial part (median 11%) of the measured surface carbon fixation can be sustained by phosphorus liberated from phosphonate utilisation, highlighting the ecological importance of phosphonates in the carbon cycle of the oligotrophic ocean.

Single-cell imaging of phosphorus uptake shows that key harmful algae rely on different phosphorus sources for growth.

Single-cell measurements of biochemical processes have advanced our understanding of cellular physiology in individual microbes and microbial populations. Due to methodological limitations, little is known about single-cell phosphorus (P) uptake and its importance for microbial growth within mixed field populations. Here, we developed a nanometer-scale secondary ion mass spectrometry (nanoSIMS)-based approach to quantify single-cell P uptake in combination with cellular CO2 and N2 fixation. Applying this approach during a harmful algal bloom (HAB), we found that the toxin-producer Nodularia almost exclusively used phosphate for growth at very low phosphate concentrations in the Baltic Sea. In contrast, the non-toxic Aphanizomenon acquired only 15% of its cellular P-demand from phosphate and ~85% from organic P. When phosphate concentrations were raised, Nodularia thrived indicating that this toxin-producer directly benefits from phosphate inputs. The phosphate availability in the Baltic Sea is projected to rise and therefore might foster more frequent and intense Nodularia blooms with a concomitant rise in the overall toxicity of HABs in the Baltic Sea. With a projected increase in HABs worldwide, the capability to use organic P may be a critical factor that not only determines the microbial community structure, but the overall harmfulness and associated costs of algal blooms.

Nutrients that limit growth in the ocean.

Phytoplankton form the basis of the marine food web and are responsible for approximately half of global carbon dioxide (CO2) fixation (∼ 50 Pg of carbon per year). Thus, these microscopic, photosynthetic organisms are vital in controlling the atmospheric CO2 concentration and Earth's climate. Phytoplankton are dependent on sunlight and their CO2-fixation activity is therefore restricted to the upper, sunlit surface ocean (that is, the euphotic zone). CO2 usually does not limit phytoplankton growth due to its high concentration in seawater. However, the vast majority of oceanic surface waters are depleted in inorganic nitrogen, phosphorus, iron and/or silica; nutrients that limit primary production in the ocean (Figure 1). Phytoplankton growth is mainly supported by either the recycling of nutrients or by reintroduction of nutrients from deeper waters by mixing. A small percentage of primary production, though, is fueled by 'external' or 'new' nutrients and it is these nutrients that determine the amount of carbon that can be sequestered long term in the deep ocean. For most nutrients such as phosphorus, iron, and silica, the external supply is limited to atmospheric deposition and/or coastal and riverine inputs, whereas their main sink is the sedimentation of particulate matter. Nitrogen, however, has an additional, biological source, the fixation of N2 gas, as well as biological sinks via the processes of denitrification and anammox. Despite the comparatively small contributions to the overall turnover of nutrients in the ocean, it is these biological processes that determine the ocean's capacity to sequester CO2 from the atmosphere on time scales of ocean circulation (∼ 1000 years). This primer will highlight shifts in the traditional paradigms of nutrient limitation in the ocean, with a focus on the uniqueness of the nitrogen cycling and its biological sources and sinks.

The effect of nutrients on carbon and nitrogen fixation by the UCYN-A-haptophyte symbiosis.

Symbiotic relationships between phytoplankton and N2-fixing microorganisms play a crucial role in marine ecosystems. The abundant and widespread unicellular cyanobacteria group A (UCYN-A) has recently been found to live symbiotically with a haptophyte. Here, we investigated the effect of nitrogen (N), phosphorus (P), iron (Fe) and Saharan dust additions on nitrogen (N2) fixation and primary production by the UCYN-A-haptophyte association in the subtropical eastern North Atlantic Ocean using nifH expression analysis and stable isotope incubations combined with single-cell measurements. N2 fixation by UCYN-A was stimulated by the addition of Fe and Saharan dust, although this was not reflected in the nifH expression. CO2 fixation by the haptophyte was stimulated by the addition of ammonium nitrate as well as Fe and Saharan dust. Intriguingly, the single-cell analysis using nanometer scale secondary ion mass spectrometry indicates that the increased CO2 fixation by the haptophyte in treatments without added fixed N is likely an indirect result of the positive effect of Fe and/or P on UCYN-A N2 fixation and the transfer of N2-derived N to the haptophyte. Our results reveal a direct linkage between the marine carbon and nitrogen cycles that is fuelled by the atmospheric deposition of dust. The comparison of single-cell rates suggests a tight coupling of nitrogen and carbon transfer that stays balanced even under changing nutrient regimes. However, it appears that the transfer of carbon from the haptophyte to UCYN-A requires a transfer of nitrogen from UCYN-A. This tight coupling indicates an obligate symbiosis of this globally important diazotrophic association.