Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies

Abstract

Trichodesmium is an important dinitrogen (N 2 )-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N 2 fixation. However, rates of these transformations and concentration gradients of N compounds in Trichodesmium colonies remain largely unresolved. We combined isotope-tracer incubations, micro-profiling and numeric modelling to explore carbon fixation, N cycling processes as well as oxygen, ammonium and nitrate concentration gradients in individual fieldsampled Trichodesmium colonies. Colonies were net-autotrophic, with carbon and N 2 fixation occurring mostly during the day. Ten percent of the fixed N was released as ammonium after 12-h incubations. Nitrification was not detectable but nitrate consumption was high when nitrate was added. The consumed nitrate was partly reduced to ammonium, while denitrification was insignificant. Thus, the potential N transformation network was characterised by fixed N gain and recycling processes rather than denitrification. Oxygen concentrations within colonies were~60-200% air-saturation. Moreover, our modelling predicted steep concentration gradients, with up to 6-fold higher ammonium concentrations, and nitrate depletion in the colony centre compared to the ambient seawater. These gradients created a chemically heterogeneous microenvironment, presumably facilitating diverse microbial metabolisms in millimetre-sized Trichodesmium colonies.

Experimentally-validated correlation analysis reveals new anaerobic methane oxidation partnerships with consortium-level heterogeneity in diazotrophy

“…This pattern may be related to variations in nitrogen supply from the external environment, as similar patterns of nutrient depletion with increasing depth into microbial aggregates have been predicted in modeling studies of nitrate uptake in Trichodesmium sp. [ 89 ] and directly observed by SIMS in stable isotope probing studies of carbon fixation in biofilm-forming filamentous cyanobacteria [ 90 ]. In these examples, modeling and experimental results document declining nitrate or bicarbonate ion availability inwards toward the center of the aggregates resulting from nitrate or bicarbonate consumption.…”

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

“…In contrast, ammonium was used and resulted in elevated percentages of symbiont-free hosts, but not a symbiont-free culture. The free-living marine cyanobacterium Trichodesmium can use NO − 3 either preferentially or concurrently during diazotrophy as an N source (Holl & Montoya, 2005;Klawonn et al, 2020;Mulholland & Capone, 2000) and other diazotrophs can simultaneously use N 2 and NO − 3 (Inomura et al, 2018). It is unusual for NO − 3 not to be used at all due to the higher overall energetic cost of nitrogen fixation added to the costs maintaining specialized cellular structures in diazotrophs (Inomura et al, 2018).…”

Peer Review #1 of "Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture (v0.1)"

“…Trichodesmium can use NO 3either preferentially or concurrently during diazotrophy as an N source (Holl & Montoya 2005;Klawonn et al 2020;Mulholland & Capone 2000) and other diazotrophs can simultaneously use N 2 and NO 3 - (Inomura et al 2018). It is unusual for NO 3not to be used at all due to the higher overall energetic cost of nitrogen fixation added to the costs maintaining specialized cellular structures in diazotrophs (Inomura et al 2018).…”