Nutrient-Colimited Trichodesmium as a Nitrogen Source or Sink in a Future Ocean

Abstract

Nitrogen-fixing (N) 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-fixer fundamentally shifts nitrogen metabolism towards organic-nitrogen scavenging following long-term high-CO adaptation under iron and/or phosphorus (co)-limitation. Global shifts in transcripts and proteins under high CO/Fe-limited and/or P-limited conditions include decreases in the N-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 growth while inhibiting N fixation. In a future high-CO ocean, this whole-cell energetic reallocation towards organic nitrogen scavenging and away from N-fixation may reduce new-nitrogen inputs by , while simultaneously depleting the scarce fixed-nitrogen supplies of nitrogen-limited open ocean ecosystems. 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 cultures adapted to high CO for 7 years followed by additional exposure to iron and/or phosphorus (co)-limitation. We show that 'future ocean' conditions of high CO and concurrent nutrient limitation(s) fundamentally shift nitrogen metabolism away from nitrogen fixation, and instead towards upregulation of organic-nitrogen scavenging pathways. We show that responses 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 towards organic nitrogen uptake and away from nitrogen fixation may substantially reduce new-nitrogen inputs by to the rest of the microbial community in the future high-CO ocean, with potential global implications for ocean carbon and nitrogen cycling.

A new mathematical model to explore microbial processes and their constraints in phytoplankton colonies and sinking marine aggregates

“…Recently, the microbial communities and potential denitrification activities associated with Trichodesmium have attracted much attention in the research community ( 32 , 33 ). The presence of potentially denitrifying microorganisms associated with Trichodesmium has raised the hypothesis that Trichodesmium may even support denitrification in its O 2 microenvironment ( 34 ), as recently demonstrated experimentally in N 2 -fixing Nodularia colonies ( 21 ). In the latter study, it was shown that a complete aerobic and anaerobic N cycle can be present in the microenvironment of Nodularia colonies.…”

Stratification, nitrogen fixation, and cyanobacterial bloom stage regulate the planktonic food web structure

“…Trichodesmium are especially favored, and their large blooms are expected to further expand under future global warming scenarios because enhanced N 2 fixation was found to persist under high CO 2 irrespective of phosphorus limitation Walworth et al, 2018). Analogously to Nodularia blooms in the Baltic Sea (Wasmund, Nausch, & Voss, 2012), blooms of Trichodesmium in other marine systems develop seasonally in association with mixing of DIN-depleted but phosphorus-rich upwelling waters into warm, stratified oceanic waters that contain seed populations of Trichodesmium (Deutsch, Sarmiento, Sigman, Gruber, & Dunne, 2007;Hegde et al, 2008;Hood, Coles, & Capone, 2004).…”

Biogenic Iron Dust: A Novel Approach to Ocean Iron Fertilization as a Means of Large Scale Removal of Carbon Dioxide From the Atmosphere

“…On the other hand, biogenic iron fertilization could have complementary effects on other aspects of nutrient limitation that ultimately affect the biological pump responsible for transport of carbon to the deep sea. It is known that Fe-limitation plays an important role in the capacity of diazotrophic cyanobacteria, for example Trichodesmium, to fix N 2 in the oligotrophic ocean (Walworth et al, 2018). Understanding how biogenic iron might affect diazotropy would be another area of useful research.…”