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1. 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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2. Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine Trichodesmium

   https://doi.org/10.1128/mSystems.00210-19  

   Inomura, Keisuke; Wilson, Samuel T.; Deutsch, Curtis (August 2019, mSystems)

   Gilbert, Jack (Ed.)

   ABSTRACT The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O 2 ) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N 2 fixation and photosynthesis. First, the model indicates that managing cellular O 2 to permit N 2 fixation requires high rates of respiratory O 2 consumption. The energetic cost amounts to ∼80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N 2 fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O 2 consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gram-negative membrane, production of extracellular polysaccharide substances (EPS), and “buffer cells” that intervene between N 2 -fixing and photosynthetic cells. Our results suggest that all three factors—respiratory protection, trichome formation, and diffusion barriers—represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen. IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates an extremely short life span of oxygen-enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis. 

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

   https://doi.org/10.1093/femsle/fnaa034  

   Benavides, Mar; Duhamel, Solange; Van Wambeke, France; Shoemaker, Katyanne M; Moisander, Pia H; Salamon, Ellen; Riemann, Lasse; Bonnet, Sophie (February 2020, FEMS Microbiology Letters)

   ABSTRACT 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. 

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4. 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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5. 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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