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 (N2) 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 N2 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 N2-fixing cyanobacterium Crocosphaera, as well as the broader ecosystem-wide implications of its activities.
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The dataset presented here resulted from the efforts of many scientists who contributed to the success of the 2015 expedition. The authors thank T. Clemente for cruise leadership of KOK1507, J. Collins, J. Ossolinski and B. Van Mooy for net trap samples used for δ15N isotope analysis and E. Boyle for support of the dissolved iron measurements. For assistance with field and laboratory work, the authors thank the operational staff of the Simons Collaboration on Ocean Processes and Ecology (SCOPE), D. Böttjer, P. Den Uyl, L. Jensen, N. Lanning, M. Linney and A. Nelson. This work was supported by grants from the Simons Foundation (no. 329108 to D.M.K. and E.F.D.), the Gordon and Betty Moore Foundation (no. 3777 to E.F.D., no. 3794 to D.M.K., no. 3776 to E.V.A.) and the Balzan Prize for Oceanography (to D.M.K.). In addition, the authors acknowledge the National Science Foundation for support of the HOT programme (OCE1260164 to M.J.C. and D.M.K.) and the Center for Microbial Oceanography: Research and Education (C-MORE; EF0424599 to D.M.K. and E.F.D.). This work is a contribution of SCOPE and C-MORE.
The authors declare no competing financial interests.
Supplementary Methods, Table and Figures. (PDF 1827 kb)
Sequencing statistics. (XLS 14 kb)
Annotation information and statistical test results for the genes analysed in this study. (XLSX 701 kb)
Normalization coefficients. (XLSX 11 kb)
Sequence data. (TXT 2136 kb)
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Wilson, S., Aylward, F., Ribalet, F. et al. Coordinated regulation of growth, activity and transcription in natural populations of the unicellular nitrogen-fixing cyanobacterium Crocosphaera. Nat Microbiol 2, 17118 (2017). https://doi.org/10.1038/nmicrobiol.2017.118
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