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1. The rate and fate of N2 and C fixation by marine diatom-diazotroph symbioses

   https://doi.org/10.1038/s41396-021-01086-7  

   Foster, Rachel A. ; Tienken, Daniela ; Littmann, Sten ; Whitehouse, Martin J. ; Kuypers, Marcel M. M. ; White, Angelicque E. ( August 2021 , The ISME Journal)

   N₂fixation constitutes an important new nitrogen source in the open sea. One group of filamentous N₂fixing cyanobacteria (Richelia intracellularis, hereafterRichelia)form symbiosis with a few genera of diatoms. High rates of N₂fixation and carbon (C) fixation have been measured in the presence of diatom-Richeliasymbioses. However, it is unknown how partners coordinate C fixation and how the symbiont sustains high rates of N₂fixation. Here, both the N₂and C fixation in wild diatom-Richeliapopulations are reported. Inhibitor experiments designed to inhibit host photosynthesis, resulted in lower estimated growth and depressed C and N₂fixation, suggesting that despite the symbionts ability to fix their own C, they must still rely on their respective hosts for C. Single cell analysis indicated that up to 22% of assimilated C in the symbiont is derived from the host, whereas 78–91% of the host N is supplied from their symbionts. A size-dependent relationship is identified where larger cells have higher N₂and C fixation, and only N₂fixation was light dependent. Using the single cell measures, the N-rich phycosphere surrounding these symbioses was estimated and contributes directly and rapidly to the surface ocean rather than the mesopelagic, even at high estimated sinking velocities (<10 m d⁻¹). Several eco-physiological parameters necessary for incorporatingmore »symbiotic N₂fixing populations into larger basin scale biogeochemical models (i.e., N and C cycles) are provided.

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2. Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture

   https://doi.org/10.7717/peerj.10115  

   Pyle, Amy E. ; Johnson, Allison M. ; Villareal, Tracy A. ( January 2020 , PeerJ)

   Nitrogen fixers (diazotrophs) are often an important nitrogen source to phytoplankton nutrient budgets in N-limited marine environments. Diazotrophic symbioses between cyanobacteria and diatoms can dominate nitrogen-fixation regionally, particularly in major river plumes and in open ocean mesoscale blooms. This study reports the successful isolation and growth in monocultures of multiple strains of a diatom-cyanobacteria symbiosis from the Gulf of Mexico using a modified artificial seawater medium. We document the influence of light and nutrients on nitrogen fixation and growth rates of the host diatom Hemiaulus hauckii Grunow together with its diazotrophic endosymbiont Richelia intracellularis Schmidt, as well as less complete results on the Hemiaulus membranaceus - R. intracellularis symbiosis. The symbioses rates reported here are for the joint diatom-cyanobacteria unit. Symbiont diazotrophy was sufficient to support both the host diatom and cyanobacteria symbionts, and the entire symbiosis replicated and grew without added nitrogen. Maximum growth rates of multiple strains of H. hauckii symbioses in N-free medium with N 2 as the sole N source were 0.74–0.93 div d −1 . Growth rates followed light saturation kinetics in H. hauckii symbioses with a growth compensation light intensity (E C ) of 7–16 µmol m −2 s −1 and saturation light levelmore »(E K ) of 84–110 µmol m −2 s −1 . Nitrogen fixation rates by the symbiont while within the host followed a diel pattern where rates increased from near-zero in the scotophase to a maximum 4–6 h into the photophase. At the onset of the scotophase, nitrogen-fixation rates declined over several hours to near-zero values. Nitrogen fixation also exhibited light saturation kinetics. Maximum N 2 fixation rates (84 fmol N 2 heterocyst −1 h −1 ) in low light adapted cultures (50 µmol m −2 s − 1) were approximately 40–50% of rates (144–154 fmol N 2 heterocyst −1 h −1 ) in high light (150 and 200 µmol m −2 s −1 ) adapted cultures. Maximum laboratory N 2 fixation rates were ~6 to 8-fold higher than literature-derived field rates of the H. hauckii symbiosis. In contrast to published results on the Rhizosolenia-Richelia symbiosis, the H. hauckii symbiosis did not use nitrate when added, although ammonium was consumed by the H. hauckii symbiosis. Symbiont-free host cell cultures could not be established; however, a symbiont-free H. hauckii strain was isolated directly from the field and grown on a nitrate-based medium that would not support DDA growth. Our observations together with literature reports raise the possibility that the asymbiotic H. hauckii are lines distinct from an obligately symbiotic H. hauckii line. While brief descriptions of successful culture isolation have been published, this report provides the first detailed description of the approaches, handling, and methodologies used for successful culture of this marine symbiosis. These techniques should permit a more widespread laboratory availability of these important marine symbioses.« less
3. 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)

   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 N₂fixation 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 N₂fixation in the Southern California Current System (SCCS) by measuring bulk community and single-cell N₂fixation 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 N₂fixation 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 N₂fixation 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). N₂fixation 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, andmore »provides evidence that the two dominant UCYN-A sublineages are separate ecotypes.

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4. Cell-specific measurements show nitrogen fixation by particle-attached putative non-cyanobacterial diazotrophs in the North Pacific Subtropical Gyre

   https://doi.org/10.1038/s41467-022-34585-y  

   Harding, Katie J. ; Turk-Kubo, Kendra A. ; Mak, Esther Wing Kwan ; Weber, Peter K. ; Mayali, Xavier ; Zehr, Jonathan P. ( November 2022 , Nature Communications)

   Biological nitrogen fixation is a major important source of nitrogen for low-nutrient surface oceanic waters. Nitrogen-fixing (diazotrophic) cyanobacteria are believed to be the primary contributors to this process, but the contribution of non-cyanobacterial diazotrophic organisms in oxygenated surface water, while hypothesized to be important, has yet to be demonstrated. In this study, we used simultaneous¹⁵N-dinitrogen and¹³C-bicarbonate incubations combined with nanoscale secondary ion mass spectrometry analysis to screen tens of thousands of mostly particle-associated, cell-like regions of interest collected from the North Pacific Subtropical Gyre. These dual isotope incubations allow us to distinguish between non-cyanobacterial and cyanobacterial nitrogen-fixing microorganisms and to measure putative cell-specific nitrogen fixation rates. With this approach, we detect nitrogen fixation by putative non-cyanobacterial diazotrophs in the oxygenated surface ocean, which are associated with organic-rich particles (<210 µm size fraction) at two out of seven locations sampled. When present, up to 4.1% of the analyzed particles contain at least one active putative non-cyanobacterial diazotroph. The putative non-cyanobacterial diazotroph nitrogen fixation rates (0.76 ± 1.60 fmol N cell⁻¹d⁻¹) suggest that these organisms are capable of fixing dinitrogen in oxygenated surface water, at least when attached to particles, and may contribute to oceanic nitrogen fixation.
5. Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters

   https://doi.org/10.1038/s41396-020-00825-6  

   Gazitúa, M. Consuelo ; Vik, Dean R. ; Roux, Simon ; Gregory, Ann C. ; Bolduc, Benjamin ; Widner, Brittany ; Mulholland, Margaret R. ; Hallam, Steven J. ; Ulloa, Osvaldo ; Sullivan, Matthew B. ( November 2020 , The ISME Journal)

   Viruses play an important role in the ecology and biogeochemistry of marine ecosystems. Beyond mortality and gene transfer, viruses can reprogram microbial metabolism during infection by expressing auxiliary metabolic genes (AMGs) involved in photosynthesis, central carbon metabolism, and nutrient cycling. While previous studies have focused on AMG diversity in the sunlit and dark ocean, less is known about the role of viruses in shaping metabolic networks along redox gradients associated with marine oxygen minimum zones (OMZs). Here, we analyzed relatively quantitative viral metagenomic datasets that profiled the oxygen gradient across Eastern Tropical South Pacific (ETSP) OMZ waters, assessing whether OMZ viruses might impact nitrogen (N) cycling via AMGs. Identified viral genomes encoded six N-cycle AMGs associated with denitrification, nitrification, assimilatory nitrate reduction, and nitrite transport. The majority of these AMGs (80%) were identified in T4-likeMyoviridaephages, predicted to infectCyanobacteriaandProteobacteria, or in unclassified archaeal viruses predicted to infectThaumarchaeota. Four AMGs were exclusive to anoxic waters and had distributions that paralleled homologous microbial genes. Together, these findings suggest viruses modulate N-cycling processes within the ETSP OMZ and may contribute to nitrogen loss throughout the global oceans thus providing a baseline for their inclusion in the ecosystem and geochemical models.