Critical Role of Light in the Growth and Activity of the Marine N2-Fixing UCYN-A Symbiosis.

The unicellular N2-fixing cyanobacteria UCYN-A live in symbiosis with haptophytes in the Braarudosphaera bigelowii lineage. Maintaining N2-fixing symbioses between two unicellular partners requires tight coordination of multiple biological processes including cell growth and division and, in the case of the UCYN-A symbiosis, N2 fixation of the symbiont and photosynthesis of the host. In this system, it is thought that the host photosynthesis supports the high energetic cost of N2 fixation, and both processes occur during the light period. However, information on this coordination is very limited and difficult to obtain because the UCYN-A symbiosis has yet to be available in culture. Natural populations containing the UCYN-A2 symbiosis were manipulated to explore the effects of alterations of regular light and dark periods and inhibition of host photosynthesis on N2 fixation (single cell N2 fixation rates), nifH gene transcription, and UCYN-A2 cell division (fluorescent in situ hybridization and nifH gene abundances). The results showed that the light period is critical for maintenance of regular patterns of gene expression, N2 fixation and symbiont replication and cell division. This study suggests a crucial role for the host as a producer of fixed carbon, rather than light itself, in the regulation and implementation of these cellular processes in UCYN-A.

UCYN-A/haptophyte symbioses dominate N2 fixation in the Southern California Current System.

The availability of fixed nitrogen (N) is an important factor limiting biological productivity in the oceans. In coastal waters, high dissolved inorganic N concentrations were historically thought to inhibit dinitrogen (N2) fixation, however, recent N2 fixation measurements and the presence of the N2-fixing UCYN-A/haptophyte symbiosis in nearshore waters challenge this paradigm. We characterized the contribution of UCYN-A symbioses to nearshore N2 fixation in the Southern California Current System (SCCS) by measuring bulk community and single-cell N2 fixation rates, as well as diazotroph community composition and abundance. UCYN-A1 and UCYN-A2 symbioses dominated diazotroph communities throughout the region during upwelling and oceanic seasons. Bulk N2 fixation was detected in most surface samples, with rates up to 23.0 ± 3.8 nmol N l-1 d-1, and was often detected at the deep chlorophyll maximum in the presence of nitrate (>1 µM). UCYN-A2 symbiosis N2 fixation rates were higher (151.1 ± 112.7 fmol N cell-1 d-1) than the UCYN-A1 symbiosis (6.6 ± 8.8 fmol N cell-1 d-1). N2 fixation by the UCYN-A1 symbiosis accounted for a majority of the measured bulk rates at two offshore stations, while the UCYN-A2 symbiosis was an important contributor in three nearshore stations. This report of active UCYN-A symbioses and broad mesoscale distribution patterns establishes UCYN-A symbioses as the dominant diazotrophs in the SCCS, where heterocyst-forming and unicellular cyanobacteria are less prevalent, and provides evidence that the two dominant UCYN-A sublineages are separate ecotypes.

Unusual marine cyanobacteria/haptophyte symbiosis relies on N2 fixation even in N-rich environments.

The microbial fixation of N2 is the largest source of biologically available nitrogen (N) to the oceans. However, it is the most energetically expensive N-acquisition process and is believed inhibited when less energetically expensive forms, like dissolved inorganic N (DIN), are available. Curiously, the cosmopolitan N2-fixing UCYN-A/haptophyte symbiosis grows in DIN-replete waters, but the sensitivity of their N2 fixation to DIN is unknown. We used stable isotope incubations, catalyzed reporter deposition fluorescence in-situ hybridization (CARD-FISH), and nanoscale secondary ion mass spectrometry (nanoSIMS), to investigate the N source used by the haptophyte host and sensitivity of UCYN-A N2 fixation in DIN-replete waters. We demonstrate that under our experimental conditions, the haptophyte hosts of two UCYN-A sublineages do not assimilate nitrate (NO3-) and meet little of their N demands via ammonium (NH4+) uptake. Instead the UCYN-A/haptophyte symbiosis relies on UCYN-A N2 fixation to supply large portions of the haptophyte's N requirements, even under DIN-replete conditions. Furthermore, UCYN-A N2 fixation rates, and haptophyte host carbon fixation rates, were at times stimulated by NO3- additions in N-limited waters suggesting a link between the activities of the bulk phytoplankton assemblage and the UCYN-A/haptophyte symbiosis. The results suggest N2 fixation may be an evolutionarily viable strategy for diazotroph-eukaryote symbioses, even in N-rich coastal or high latitude waters.

Kilauea lava fuels phytoplankton bloom in the North Pacific Ocean.

From June to August 2018, the eruption of Kilauea volcano on the island of Hawai'i injected millions of cubic meters of molten lava into the nutrient-poor waters of the North Pacific Subtropical Gyre. The lava-impacted seawater was characterized by high concentrations of metals and nutrients that stimulated phytoplankton growth, resulting in an extensive plume of chlorophyll a that was detectable by satellite. Chemical and molecular evidence revealed that this biological response hinged on unexpectedly high concentrations of nitrate, despite the negligible quantities of nitrogen in basaltic lava. We hypothesize that the high nitrate was caused by buoyant plumes of nutrient-rich deep waters created by the substantial input of lava into the ocean. This large-scale ocean fertilization was therefore a unique perturbation event that revealed how marine ecosystems respond to exogenous inputs of nutrients.

Distributions and Abundances of Sublineages of the N2-Fixing Cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A) in the New Caledonian Coral Lagoon.

Nitrogen (N2) fixation is a major source of nitrogen that supports primary production in the vast oligotrophic areas of the world's oceans. The Western Tropical South Pacific has recently been identified as a hotspot for N2 fixation. In the Noumea lagoon (New Caledonia), high abundances of the unicellular N2-fixing cyanobacteria group A (UCYN-A), coupled with daytime N2 fixation rates associated with the <10 µm size fraction, suggest UCYN-A may be an important diazotroph (N2-fixer) in this region. However, little is known about the seasonal variability and diversity of UCYN-A there. To assess this, surface waters from a 12 km transect from the mouth of the Dumbea River to the Dumbea Pass were sampled monthly between July 2012 and March 2014. UCYN-A abundances for two of the defined sublineages, UCYN-A1 and UCYN-A2, were quantified using qPCR targeting the nifH gene, and the nifH-based diversity of UCYN-A was characterized by identifying oligotypes, alternative taxonomic units defined by nucleotide positions with high variability. UCYN-A abundances were dominated by the UCYN-A1 sublineage, peaked in September and October and could be predicted by a suite of nine environmental parameters. At the sublineage level, UCYN-A1 abundances could be predicted based on lower temperatures (<23°C), nitrate concentrations, precipitation, wind speed, while UCYN-A2 abundances could be predicted based on silica, and chlorophyll a concentrations, wind direction, precipitation, and wind speed. Using UCYN-A nifH oligotyping, similar environmental variables explained the relative abundances of sublineages and their associated oligotypes, with the notable exception of the UCYN-A2 oligotype (oligo43) which had relative abundance patterns distinct from the dominant UCYN-A2 oligotype (oligo3). The results support an emerging pattern that UCYN-A is comprised of a diverse group of strains, with sublineages that may have different ecological niches. By identifying environmental factors that influence the composition and abundance of UCYN-A sublineages, this study helps to explain global UCYN-A abundance patterns, and is important for understanding the significance of N2 fixation at local and global scales.