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

Nature Microbiology volume 2, Article number: 17118 (2017) Cite this article

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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 (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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Figure 1: High Crocosphaera abundances located in an anticyclonic eddy coinciding with elevated water column chlorophyll a and productivity.
Figure 2: Sub-populations of Crocosphaera.
Figure 3: Transcriptional network of Crocosphaera.
Figure 4: Diel cascade in Crocosphaera transcripts.
Figure 5: Diel patterns in Crocosphaera abundances and N2 fixation alongside transcript abundances for key genes.

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Acknowledgements

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.

Author information

Author notes

  1. Frank O. Aylward

    Present address: Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, 24061, USA

  2. Matthew J. Church

    Present address: Flathead Lake Biological Station, University of Montana, Polson, Montana, 59860, USA

  3. Samuel T. Wilson and Frank O. Aylward: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Oceanography, Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii, Honolulu, 96822, Hawaii, USA

    Samuel T. Wilson, Frank O. Aylward, Benedetto Barone, John R. Casey, John M. Eppley, Sara Ferrón, Anna E. Romano, Alice Vislova, Matthew J. Church, David M. Karl & Edward F. DeLong

  2. School of Oceanography, University of Washington, Seattle, 98195, Washington, USA

    Francois Ribalet & E. Virginia Armbrust

  3. Department of Biological Sciences, University of Southern California, Los Angeles, 90089, California, USA

    Paige E. Connell & David A. Caron

  4. Department of Oceanography, Texas A&M University, College Station, 77843, Texas, USA

    Jessica N. Fitzsimmons

  5. School of Ocean Science and Technology, University of Southern Mississippi, Stennis Space Center, 39529, Mississippi, USA

    Christopher T. Hayes

  6. Ocean Sciences Department, University of California, Santa Cruz, 95064, California, USA

    Kendra A. Turk-Kubo & Jonathan P. Zehr

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Contributions

All authors contributed to the design of the study. S.T.W. and D.M.K. measured nitrogen fixation and provided the water-column hydrography and biogeochemical data. F.O.A., A.E.R., A.V., J.M.E. and E.F.D. sampled, prepared and analysed the metatranscriptomic and metagenomic data. F.R. and E.V.A. conducted the underway enumeration of Crocosphaera abundances. B.B. and F.R. quantified the abundances of larger size Crocosphaera. D.A.C. and P.E.C. performed the microscopy analyses and dilution grazing experiments. S.F. and J.R.C. conducted the productivity measurements. M.J.C. provided the time-series nifH abundances and measured particle export. J.R.C. and B.B. collected and analysed the isotopic composition of sinking particles. K.A.T.-K. and J.P.Z. analysed the nifH abundances. C.T.H. and J.N.F. measured dissolved iron concentrations. S.T.W., F.O.A., D.M.K. and E.F.D. wrote the manuscript with contributions from all coauthors.

Corresponding author

Correspondence to Edward F. DeLong.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Table and Figures. (PDF 1827 kb)

Supplementary Dataset 1

Sequencing statistics. (XLS 14 kb)

Supplementary Dataset 2

Annotation information and statistical test results for the genes analysed in this study. (XLSX 701 kb)

Supplementary Dataset 3

Normalization coefficients. (XLSX 11 kb)

Supplementary Dataset 4

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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