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

   https://doi.org/10.1038/s43705-021-00039-7  

   Turk-Kubo, Kendra A.; Mills, Matthew M.; Arrigo, Kevin R.; van Dijken, Gert; Henke, Britt A.; Stewart, Brittany; Wilson, Samuel T.; Zehr, Jonathan P. (August 2021, ISME Communications)

   Abstract 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. 

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

   https://doi.org/10.1038/s41396-020-0691-6  

   Mills, Matthew M.; Turk-Kubo, Kendra A.; van Dijken, Gert L.; Henke, Britt A.; Harding, Katie; Wilson, Samuel T.; Arrigo, Kevin R.; Zehr, Jonathan P. (October 2020, The ISME Journal)

   null (Ed.)

   Abstract The microbial fixation of N 2 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 N 2 -fixing UCYN-A/haptophyte symbiosis grows in DIN-replete waters, but the sensitivity of their N 2 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 N 2 fixation in DIN-replete waters. We demonstrate that under our experimental conditions, the haptophyte hosts of two UCYN-A sublineages do not assimilate nitrate (NO 3 − ) and meet little of their N demands via ammonium (NH 4 + ) uptake. Instead the UCYN-A/haptophyte symbiosis relies on UCYN-A N 2 fixation to supply large portions of the haptophyte’s N requirements, even under DIN-replete conditions. Furthermore, UCYN-A N 2 fixation rates, and haptophyte host carbon fixation rates, were at times stimulated by NO 3 − 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 N 2 fixation may be an evolutionarily viable strategy for diazotroph–eukaryote symbioses, even in N-rich coastal or high latitude waters. 

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3. Open ocean and coastal strains of the N2-fixing cyanobacterium UCYN-A have distinct transcriptomes

   https://doi.org/10.1371/journal.pone.0272674  

   Muñoz-Marín, María_del Carmen; Magasin, Jonathan D; Zehr, Jonathan P (May 2023, PLOS ONE)

   Kothe, Erika (Ed.)

   Decades of research on marine N₂fixation focused onTrichodesmium, which are generally free-living cyanobacteria, but in recent years the endosymbiotic cyanobacteriumCandidatusAtelocyanobacterium thalassa (UCYN-A) has received increasing attention. However, few studies have shed light on the influence of the host versus the habitat on UCYN-A N₂fixation and overall metabolism. Here we compared transcriptomes from natural populations of UCYN-A from oligotrophic open-ocean versus nutrient-rich coastal waters, using a microarray that targets the full genomes of UCYN-A1 and UCYN-A2 and known genes for UCYN-A3. We found that UCYN-A2, usually regarded as adapted to coastal environments, was transcriptionally very active in the open ocean and appeared to be less impacted by habitat change than UCYN-A1. Moreover, for genes with 24 h periodic expression we observed strong but inverse correlations among UCYN-A1, A2, and A3 to oxygen and chlorophyll, which suggests distinct host-symbiont relationships. Across habitats and sublineages, genes for N₂fixation and energy production had high transcript levels, and, intriguingly, were among the minority of genes that kept the same schedule of diel expression. This might indicate different regulatory mechanisms for genes that are critical to the symbiosis for the exchange of nitrogen for carbon from the host. Our results underscore the importance of N₂fixation in UCYN-A symbioses across habitats, with consequences for community interactions and global biogeochemical cycles. 

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4. Elucidation of trophic interactions in an unusual single-cell nitrogen-fixing symbiosis using metabolic modeling

   https://doi.org/10.1371/journal.pcbi.1008983  

   Sarkar, Debolina; Landa, Marine; Bandyopadhyay, Anindita; Pakrasi, Himadri B.; Zehr, Jonathan P.; Maranas, Costas D. (May 2021, PLOS Computational Biology)

   Hatzimanikatis, Vassily (Ed.)

   Marine nitrogen-fixing microorganisms are an important source of fixed nitrogen in oceanic ecosystems. The colonial cyanobacterium Trichodesmium and diatom symbionts were thought to be the primary contributors to oceanic N 2 fixation until the discovery of the unusual uncultivated symbiotic cyanobacterium UCYN-A ( Candidatus Atelocyanobacterium thalassa ). UCYN-A has atypical metabolic characteristics lacking the oxygen-evolving photosystem II, the tricarboxylic acid cycle, the carbon-fixation enzyme RuBisCo and de novo biosynthetic pathways for a number of amino acids and nucleotides. Therefore, it is obligately symbiotic with its single-celled haptophyte algal host. UCYN-A receives fixed carbon from its host and returns fixed nitrogen, but further insights into this symbiosis are precluded by both UCYN-A and its host being uncultured. In order to investigate how this syntrophy is coordinated, we reconstructed bottom-up genome-scale metabolic models of UCYN-A and its algal partner to explore possible trophic scenarios, focusing on nitrogen fixation and biomass synthesis. Since both partners are uncultivated and only the genome sequence of UCYN-A is available, we used the phylogenetically related Chrysochromulina tobin as a proxy for the host. Through the use of flux balance analysis (FBA), we determined the minimal set of metabolites and biochemical functions that must be shared between the two organisms to ensure viability and growth. We quantitatively investigated the metabolic characteristics that facilitate daytime N 2 fixation in UCYN-A and possible oxygen-scavenging mechanisms needed to create an anaerobic environment to allow nitrogenase to function. This is the first application of an FBA framework to examine the tight metabolic coupling between uncultivated microbes in marine symbiotic communities and provides a roadmap for future efforts focusing on such specialized systems. 

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5. Nitrogen fixation rates in the Guinea Dome and the equatorial upwelling regions in the Atlantic Ocean

   https://doi.org/10.1007/s10533-023-01089-w  

   Fernández-Carrera, Ana; Kiko, Rainer; Hauss, Helena; Hamilton, Douglas S.; Achterberg, Eric P.; Montoya, Joseph P.; Dengler, Marcus; Brandt, Peter; Subramaniam, Ajit (December 2023, Biogeochemistry)

   Abstract Biological nitrogen fixation is a key process balancing the loss of combined nitrogen in the marine nitrogen cycle. Its relevance in upwelling or high nutrient regions is still unclear, with the few available studies in these regions of the ocean reporting rates that vary widely from below detection limit to > 100 nmol N L⁻¹ d⁻¹. In the eastern tropical Atlantic Ocean, two open ocean upwelling systems are active in boreal summer. One is the seasonal equatorial upwelling, where the residual phosphorus associated with aged upwelled waters is suggested to enhance nitrogen fixation in this season. The other is the Guinea Dome, a thermal upwelling dome. We conducted two surveys along 23° W across the Guinea Dome and the Equator from 15° N to 5° S in September 2015 and August–September 2016 with high latitudinal resolution (20–60 nm between stations). The abundance ofTrichodesmiumcolonies was characterized by an Underwater Vision Profiler 5 and the total biological nitrogen fixation in the euphotic layer was measured using the¹⁵N₂technique. The highest abundances ofTrichodesmiumcolonies were found in the area of the Guinea Dome (9°–15° N) with a maximum of 3 colonies L⁻¹near the surface. By contrast, colonies were almost absent in the Equatorial band between 2° N and 5° S. The highest nitrogen fixation rate was measured at the northern edge of the Guinea Dome in 2016 (ca. 31 nmol N L⁻¹ d⁻¹). In this region, where diazotrophs thrived on a sufficient supply of both phosphorus and iron, a patchy distribution was unveiled by our increased spatial resolution scheme. In the Equatorial band, rates were considerably lower, ranging from below detection limit to ca. 4 nmol N L⁻¹ d⁻¹, with a clear difference in magnitude between 2015 (rates close to zero) and 2016 (average rates around 2 nmol N L⁻¹ d⁻¹). This difference seemed triggered by a contrasting supply of phosphorus between years. Our study stresses the importance of surveys with sampling at fine-scale spatial resolution, and shows unexpected high variability in the rates of nitrogen fixation in the Guinea Dome, a region where diazotrophy is a significant process supplying new nitrogen into the euphotic layer. 

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