Coordinated regulation of growth, activity and transcription in natural populations of the unicellular nitrogen-fixing cyanobacterium Crocosphaera

Abstract

The temporal dynamics of phytoplankton growth and activity have large impacts on fluxes of matter and energy, yet obtaining in situ metabolic measurements of sufficient resolution for even dominant microorganisms remains a considerable challenge. We performed Lagrangian diel sampling with synoptic measurements of population abundances, dinitrogen (N) fixation, mortality, productivity, export and transcription in a bloom of Crocosphaera over eight days in the North Pacific Subtropical Gyre (NPSG). Quantitative transcriptomic analyses revealed clear diel oscillations in transcript abundances for 34% of Crocosphaera genes identified, reflecting a systematic progression of gene expression in diverse metabolic pathways. Significant time-lagged correspondence was evident between nifH transcript abundance and maximal N fixation, as well as sepF transcript abundance and cell division, demonstrating the utility of transcriptomics to predict the occurrence and timing of physiological and biogeochemical processes in natural populations. Indirect estimates of carbon fixation by Crocosphaera were equivalent to 11% of net community production, suggesting that under bloom conditions this diazotroph has a considerable impact on the wider carbon cycle. Our cross-scale synthesis of molecular, population and community-wide data underscores the tightly coordinated in situ metabolism of the keystone N-fixing cyanobacterium Crocosphaera, as well as the broader ecosystem-wide implications of its activities.

Nitrogen fixation rates diagnosed from diurnal changes in elemental stoichiometry

“…Although the average nitrogen fixation measured with traditional methods is comparable to that inferred from stoichiometry, the peak fixation occurs at night for the isotope method whereas stoichiometry predicts a strong peak during the day. The nighttime peak found by traditional methods is consistent with the large amount of Crocosphaera found during the cruise (Wilson et al ) and Crocosphaera are known to fix nitrogen at night (Zehr ). The nitrogen fixation time series inferred from stoichiometry has no nighttime peak because Crocosphaera is not concentrated by sampling the > 20 μm size fraction.…”

“…During our field campaign, nitrogen fixation was also measured across the diurnal cycle (Wilson et al ) using the 15 N isotope tracer technique (Mohr et al ; Wilson et al ). Details of these measurements and their relation to diazotrophic community structure can be found in Wilson et al (). These measurements were conducted using water collected from 15 m; were made at approximately 4 h intervals; and were conducted in deck board incubations, under simulated light conditions.…”

“… Comparison of measured fixation ( ) rates with those diagnosed for the 20–200 mm size fraction from elemental ratios (red filled circles). The 15 N derived curve peaks at nighttime, likely due to Crocosphaera (Wilson et al ) while the large size fraction peaks during the daytime. This is consistent with solar irradiation driving nitrogen fixation in DDAs and Trichodesmium .…”

“…Time series of nitrogen fixation were also estimated via measurement of assimilation in bottle incubations (Wilson et al ). Rates of assimilation were conducted using ‐labeled gas (Cambridge Isotope Laboratories) dissolved in filtered seawater prior to its addition.…”

Dynamics of phytoplankton and heterotrophic bacterioplankton in the western tropical South Pacific Ocean along a gradient of diversity and activity of diazotrophs

“…One of its sub-populations is recognized to produce EPS (Bench et al, 2016), which could be a significant energy source for heterotrophic prokaryotes. In the North Pacific Subtropical gyre, Wilson et al (2017) hypothesized that Crocosphaera could fix N 2 in excess of its growth requirements and could leak fixed N from the cells. They also showed a highly dynamic of Crocosphaera growth and decay during diel 570 cycles survey, suggesting efficient mortality sources.…”