skip to main content


Title: Nutrient-Colimited Trichodesmium as a Nitrogen Source or Sink in a Future Ocean
ABSTRACT Nitrogen-fixing (N 2 ) cyanobacteria provide bioavailable nitrogen to vast ocean regions but are in turn limited by iron (Fe) and/or phosphorus (P), which may force them to employ alternative nitrogen acquisition strategies. The adaptive responses of nitrogen fixers to global-change drivers under nutrient-limited conditions could profoundly alter the current ocean nitrogen and carbon cycles. Here, we show that the globally important N 2 fixer Trichodesmium fundamentally shifts nitrogen metabolism toward organic-nitrogen scavenging following long-term high-CO 2 adaptation under iron and/or phosphorus (co)limitation. Global shifts in transcripts and proteins under high-CO 2 /Fe-limited and/or P-limited conditions include decreases in the N 2 -fixing nitrogenase enzyme, coupled with major increases in enzymes that oxidize trimethylamine (TMA). TMA is an abundant, biogeochemically important organic nitrogen compound that supports rapid Trichodesmium growth while inhibiting N 2 fixation. In a future high-CO 2 ocean, this whole-cell energetic reallocation toward organic nitrogen scavenging and away from N 2 fixation may reduce new-nitrogen inputs by Trichodesmium while simultaneously depleting the scarce fixed-nitrogen supplies of nitrogen-limited open-ocean ecosystems. IMPORTANCE Trichodesmium is among the most biogeochemically significant microorganisms in the ocean, since it supplies up to 50% of the new nitrogen supporting open-ocean food webs. We used Trichodesmium cultures adapted to high-CO 2 conditions for 7 years, followed by additional exposure to iron and/or phosphorus (co)limitation. We show that “future ocean” conditions of high CO 2 and concurrent nutrient limitation(s) fundamentally shift nitrogen metabolism away from nitrogen fixation and instead toward upregulation of organic nitrogen-scavenging pathways. We show that the responses of Trichodesmium to projected future ocean conditions include decreases in the nitrogen-fixing nitrogenase enzymes coupled with major increases in enzymes that oxidize the abundant organic nitrogen source trimethylamine (TMA). Such a shift toward organic nitrogen uptake and away from nitrogen fixation may substantially reduce new-nitrogen inputs by Trichodesmium to the rest of the microbial community in the future high-CO 2 ocean, with potential global implications for ocean carbon and nitrogen cycling.  more » « less
Award ID(s):
1657757 1260490
NSF-PAR ID:
10049810
Author(s) / Creator(s):
; ; ; ; ; ; ;
Date Published:
Journal Name:
Applied and Environmental Microbiology
Volume:
84
Issue:
3
ISSN:
0099-2240
Page Range / eLocation ID:
e02137-17
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Increased stratification and mixed layer shoaling of the surface ocean resulting from warming can lead to exposure of marine dinitrogen (N2)‐fixing cyanobacteria to higher levels of inhibitory ultraviolet (UV) radiation. These same processes also reduce vertically advected supplies of the potentially limiting nutrient phosphorus (P) to N2fixers. It is currently unknown how UV inhibition and P limitation interact to affect the biogeochemical cycles of nitrogen and carbon in these biogeochemically critical microbes. We investigated the responses of the important and widespread marine N2‐fixing cyanobacteriaCrocosphaera(strain WH0005) andTrichodesmium(strains IMS 101 and GBR) to UV‐A and UV‐B under P‐replete and P‐limited conditions. Growth, N2fixation, and carbon dioxide (CO2) fixation rates ofTrichodesmiumIMS 101 andCrocosphaerawere negatively affected by UV exposure. This inhibition was greater forTrichodesmiumIMS 101 than forCrocosphaera, which fixes N2only during the night and so avoids direct UV damage. Negative effects of UV on both IMS 101 andCrocosphaerawere less in P‐limited cultures than in P‐replete cultures. In contrast, no UV inhibition was observed in GBR, regardless of P availability. UV inhibition was related to different amounts of UV‐absorbing compounds produced by these isolates. Responses to UV radiation and P availability interactions were taxon‐specific, but our results indicated that in general, UV radiation effects onTrichodesmiumandCrocosphaerarange from negative to neutral. UV inhibition and its interactions with P limitation may thus have a substantial influence on the present day and future nitrogen and carbon cycles of the ocean.

     
    more » « less
  2. 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. 
    more » « less
  3. Summary

    In the surface waters of the warm oligotrophic ocean, filaments and aggregated colonies of the nitrogen (N)‐fixing cyanobacteriumTrichodesmiumcreate microscale nutrient‐rich oases. These hotspots fuel primary productivity and harbour a diverse consortium of heterotrophs. Interactions with associated microbiota can affect the physiology ofTrichodesmium, often in ways that have been predicted to support its growth. Recently, it was found that trimethylamine (TMA), a globally abundant organic N compound, inhibits N2fixation in cultures ofTrichodesmiumwithout impairing growth rate, suggesting thatTrichodesmiumcan use TMA as an alternate N source. In this study,15N‐TMA DNA stable isotope probing (SIP) of aTrichodesmiumenrichment was employed to further investigate TMA metabolism and determine whether TMA‐N is incorporated directly or secondarily via cross‐feeding facilitated by microbial associates. Herein, we identify two members of the marineRoseobacterclade (MRC) of Alphaproteobacteria as the likely metabolizers of TMA and provide genomic evidence that they converted TMA into a more readily available form of N, e.g., ammonium (NH4+), which was subsequently used byTrichodesmiumand the rest of the community. The results implicate microbiome‐mediated carbon (C) and N transformations in modulating N2fixation and thus highlight the involvement of host‐associated heterotrophs in global biogeochemical cycling.

     
    more » « less
  4. Abstract. Trichodesmium is a globally important marine microbe that provides fixednitrogen (N) to otherwise N-limited ecosystems. In nature, nitrogen fixationis likely regulated by iron or phosphate availability, but the extent andinteraction of these controls are unclear. From metaproteomics analysesusing established protein biomarkers for nutrient stress, we foundthat iron–phosphate co-stress is the norm rather than the exception for Trichodesmium colonies in theNorth Atlantic Ocean. Counterintuitively, the nitrogenase enzyme was moreabundant under co-stress as opposed to single nutrient stress. This isconsistent with the idea that Trichodesmium has a specific physiological state duringnutrient co-stress. Organic nitrogen uptake was observed and occurredsimultaneously with nitrogen fixation. The quantification of the phosphate ABCtransporter PstA combined with a cellular model of nutrient uptake suggestedthat Trichodesmium is generally confronted by the biophysical limits of membrane spaceand diffusion rates for iron and phosphate acquisition in the field. Colonyformation may benefit nutrient acquisition from particulate and organicsources, alleviating these pressures. The results highlight that topredict the behavior of Trichodesmium, both Fe and P stress must be evaluatedsimultaneously. 
    more » « less
  5. The oceanic dissolved organic phosphorus (DOP) pool is mainly composed of P-esters and, to a lesser extent, equally abundant phosphonate and P-anhydride molecules. In phosphate-limited ocean regions, diazotrophs are thought to rely on DOP compounds as an alternative source of phosphorus (P). While both P-esters and phosphonates effectively promote dinitrogen (N 2 ) fixation, the role of P-anhydrides for diazotrophs is unknown. Here we explore the effect of P-anhydrides on N 2 fixation at two stations with contrasting biogeochemical conditions: one located in the Tonga trench volcanic arc region (“volcano,” with low phosphate and high iron concentrations), and the other in the South Pacific Gyre (“gyre,” with moderate phosphate and low iron). We incubated surface seawater with AMP (P-ester), ATP (P-ester and P-anhydride), or 3polyP (P-anhydride) and determined cell-specific N 2 fixation rates, nifH gene abundance, and transcription in Crocosphaera and Trichodesmium . Trichodesmium did not respond to any DOP compounds added, suggesting that they were not P-limited at the volcano station and were outcompeted by the low iron conditions at the gyre station. Conversely, Crocosphaera were numerous at both stations and their specific N 2 fixation rates were stimulated by AMP at the volcano station and slightly by 3polyP at both stations. Heterotrophic bacteria responded to ATP and 3polyP additions similarly at both stations, despite the contrasting phosphate and iron availability. The use of 3polyP by Crocosphaera and heterotrophic bacteria at both low and moderate phosphate concentrations suggests that this compound, in addition to being a source of P, can be used to acquire energy for which both groups compete. P-anhydrides may thus leverage energy restrictions to diazotrophs in the future stratified and nutrient-impoverished ocean. 
    more » « less