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1. Quantitative Analysis of the Trade-Offs of Colony Formation for Trichodesmium

   https://doi.org/10.1128/spectrum.02025-22  

   Agarwal, Vitul ; Inomura, Keisuke ; Mouw, Colleen B. ( December 2022 , Microbiology Spectrum)

   Veach, Allison (Ed.)

   ABSTRACT There is considerable debate about the benefits and trade-offs for colony formation in a major marine nitrogen fixer, Trichodesmium . To quantitatively analyze the trade-offs, we developed a metabolic model based on carbon fluxes to compare the performance of Trichodesmium colonies and free trichomes under different scenarios. Despite reported reductions in carbon fixation and nitrogen fixation rates for colonies relative to free trichomes, we found that model colonies can outperform individual cells in several cases. The formation of colonies can be advantageous when respiration rates account for a high proportion of the carbon fixation rate. Negative external influence on vital rates, such as mortality due to predation or micronutrient limitations, can also create a net benefit for colony formation relative to individual cells. In contrast, free trichomes also outcompete colonies in many scenarios, such as when respiration rates are equal for both colonies and individual cells or when there is a net positive external influence on rate processes (i.e., optimal environmental conditions regarding light and temperature or high nutrient availability). For both colonies and free trichomes, an increase in carbon fixation relative to nitrogen fixation rates would increase their relative competitiveness. These findings suggest that the formation of colonies in Trichodesmium might be linked to specific environmental and ecological circumstances. Our results provide a road map for empirical studies and models to evaluate the conditions under which colony formation in marine phytoplankton can be sustained in the natural environment. IMPORTANCE Trichodesmium is a marine filamentous cyanobacterium that fixes nitrogen and is an important contributor to the global nitrogen cycle. In the natural environment, Trichodesmium can exist as individual cells (trichomes) or as colonies (puffs and tufts). In this paper, we try to answer a longstanding question in marine microbial ecology: how does colony formation benefit the survival of Trichodesmium ? To answer this question, we developed a carbon flux model that utilizes existing published rates to evaluate whether and when colony formation can be sustained. Enhanced respiration rates, influential external factors such as environmental conditions and ecological interactions, and variable carbon and nitrogen fixation rates can all create scenarios for colony formation to be a viable strategy. Our results show that colony formation is an ecologically beneficial strategy under specific conditions, enabling Trichodesmium to be a globally significant organism. 

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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. Altered growth and death in dilution-based viral predation assays

   https://doi.org/10.1371/journal.pone.0288114  

   Knowles, Ben ; Bonachela, Juan A. ; Cieslik, Nick ; Della Penna, Alice ; Diaz, Ben ; Baetge, Nick ; Behrenfeld, Micheal J. ; Naumovitz, Karen ; Boss, Emmanuel ; Graff, Jason R. ; et al ( July 2023 , PLOS ONE)

   Chen, Peng (Ed.)

   Viral lysis of phytoplankton is one of the most common forms of death on Earth. Building on an assay used extensively to assess rates of phytoplankton loss to predation by grazers, lysis rates are increasingly quantified through dilution-based techniques. In this approach, dilution of viruses and hosts are expected to reduce infection rates and thus increase host net growth rates (i.e., accumulation rates). The difference between diluted and undiluted host growth rates is interpreted as a measurable proxy for the rate of viral lytic death. These assays are usually conducted in volumes ≥ 1 L. To increase throughput, we implemented a miniaturized, high-throughput, high-replication, flow cytometric microplate dilution assay to measure viral lysis in environmental samples sourced from a suburban pond and the North Atlantic Ocean. The most notable outcome we observed was a decline in phytoplankton densities that was exacerbated by dilution, instead of the increased growth rates expected from lowered virus-phytoplankton encounters. We sought to explain this counterintuitive outcome using theoretical, environmental, and experimental analyses. Our study shows that, while die-offs could be partly explained by a ‘plate effect’ due to small incubation volumes and cells adhering to walls, the declines in phytoplankton densities are not volume-dependent. Rather, they are driven by many density- and physiology-dependent effects of dilution on predation pressure, nutrient limitation, and growth, all of which violate the original assumptions of dilution assays. As these effects are volume-independent, these processes likely occur in all dilution assays that our analyses show to be remarkably sensitive to dilution-altered phytoplankton growth and insensitive to actual predation pressure. Incorporating altered growth as well as predation, we present a logical framework that categorizes locations by the relative dominance of these mechanisms, with general applicability to dilution-based assays.

    

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4. Image‐based root phenotyping links root architecture to micronutrient concentration in cassava

   https://doi.org/10.1002/ppp3.10130  

   Busener, Natalie ; Kengkanna, Jitrana ; Saengwilai, Patompong Johns ; Bucksch, Alexander ( July 2020 , PLANTS, PEOPLE, PLANET)

   Micronutrient deficiency or “hidden hunger” is estimated to affect two billion people worldwide and increasing the micronutrient concentration of food could play an important role in tackling this global challenge. Using a combination of imaging techniques and atomic absorption spectroscopy, we describe a link between root phenotype and micronutrient concentration in cassava, which could enable new phenotypic selection strategies for breeding. This approach could be used with existing breeding infrastructure to enhance the micronutrient concentration of cassava and hence, benefit the health of people, particularly in low‐income countries where cassava is consumed as a staple crop.

   Cassava storage roots are a staple food in low‐income countries of South‐East Asia and sub‐Saharan Africa, where growth stunting is prevalent as a consequence of micronutrient deficiencies. We aim to link phenotypes of field‐grown cassava roots to micronutrient concentration in the edible storage roots as a simple way to improve phenotypic selection for nutritional value in cassava.

   We used existing and newly developed imaging techniques to quantify root phenotypes of the cassava root architecture over time and used flame atomic absorption spectroscopy to measure micronutrient concentration in storage roots. Both together allow the association of root phenotypes with micronutrient concentration in mature cassava roots.

   We show that early and late bulking genotypes in cassava exhibit distinct foraging behaviors that are associated with micronutrient concentration in the edible storage root. Our observations suggest that late bulking cassava is a key to provide sufficient micronutrients in the edible storage root.

   The association between root phenotype and micronutrient concentration with imaging techniques allows phenotypic selection for enhanced micronutrient concentration. Therefore, implementing image‐based phenotyping into cassava breeding programs in sub‐Saharan Africa and South‐East Asia could be an essential element to resolve micronutrient deficiencies that puts individuals at a higher risk of growth stunting.

    

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5. Iron “ore” nothing: benthic iron fluxes from the oxygen-deficient Santa Barbara Basin enhance phytoplankton productivity in surface waters

   https://doi.org/10.5194/bg-21-773-2024  

   Robinson, De'Marcus ; Pham, Anh L. ; Yousavich, David J. ; Janssen, Felix ; Wenzhöfer, Frank ; Arrington, Eleanor C. ; Gosselin, Kelsey M. ; Sandoval-Belmar, Marco ; Mar, Matthew ; Valentine, David L. ; et al ( February 2024 , Biogeosciences)

   Abstract. The trace metal iron (Fe) is an essential micronutrient that controls phytoplankton productivity, which subsequently affects organic matter cycling with feedback on the cycling of macronutrients. Along the continental margin of the US West Coast, high benthic Fe release has been documented, in particular from deep anoxic basins in the Southern California Borderland. However, the influence of this Fe release on surface primary production remains poorly understood. In the present study from the Santa Barbara Basin, in situ benthic Fe fluxes were determined along a transect from shallow to deep sites in the basin. Fluxes ranged between 0.23 and 4.9 mmol m−2 d−1, representing some of the highest benthic Fe fluxes reported to date. To investigate the influence of benthic Fe release from the oxygen-deficient deep basin on surface phytoplankton production, we combined benthic flux measurements with numerical simulations using the Regional Ocean Modeling System coupled to the Biogeochemical Elemental Cycling (ROMS-BEC) model. For this purpose, we updated the model Fe flux parameterization to include the new benthic flux measurements from the Santa Barbara Basin. Our simulations suggest that benthic Fe fluxes enhance surface primary production, supporting a positive feedback on benthic Fe release by decreasing oxygen in bottom waters. However, a reduction in phytoplankton Fe limitation by enhanced benthic fluxes near the coast may be partially compensated for by increased nitrogen limitation further offshore, limiting the efficacy of this positive feedback.

    

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