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Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom

Abstract

Marine phytoplankton perform approximately half of global carbon fixation, with their blooms contributing disproportionately to carbon sequestration1, and most phytoplankton production is ultimately consumed by heterotrophic prokaryotes2. Therefore, phytoplankton and heterotrophic community dynamics are important in modelling carbon cycling and the impacts of global change3. In a typical bloom, diatoms dominate initially, transitioning over several weeks to smaller and motile phytoplankton4. Here, we show unexpected, rapid community variation from daily rRNA analysis of phytoplankton and prokaryotic community members following a bloom off southern California. Analysis of phytoplankton chloroplast 16S rRNA demonstrated ten different dominant phytoplankton over 18 days alone, including four taxa with animal toxin-producing strains. The dominant diatoms, flagellates and picophytoplankton varied dramatically in carbon export potential. Dominant prokaryotes also varied rapidly. Euryarchaea briefly became the most abundant organism, peaking over a few days to account for about 40% of prokaryotes. Phytoplankton and prokaryotic communities correlated better with each other than with environmental parameters. Extending beyond the traditional view of blooms being controlled primarily by physics and inorganic nutrients, these dynamics imply highly heterogeneous, continually changing conditions over time and/or space and suggest that interactions among microorganisms are critical in controlling plankton diversity, dynamics and fates.

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Figure 1: Dynamics of eukaryotic phytoplankton taxa (99% operational taxonomic units (OTUs)) as measured by 16S rRNA sequences of chloroplasts.
Figure 2: Dynamics of bacterial and archaeal 99% OTUs.
Figure 3: Correlations among biotic and abiotic parameters indicate stronger relationships between populations of microorganisms than to other bulk environmental parameters.

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Acknowledgements

The authors acknowledge the USC Wrigley Institute of Environmental Science and thank R. Marinelli, S. Conner, G. Boivin and the crew of the Miss Christie for sampling opportunities and laboratory space, and J. Chang, C. Chow, A. Lie, S. McCallister and E. Teel for sampling assistance. The authors thank D. Caron, F. Corsetti, J. Heidelberg, E. Webb, N. Ahlgren, L. Berdjeb, J. Cram, D. Comeau, L. Gómez Consarnau, E. Fichot, M. Lee, A. Parada, B. Phillips, G. Ramirez and E. Sieradzki for discussion and feedback on the manuscript, along with R. Sachdeva who also provided computer support. This work was supported by NSF grants 1031743 and 1136818, grant GBMF3779 from the Gordon and Betty Moore Foundation Marine Microbiology Initiative and a National Science Foundation Graduate Student Research Fellowship to D.M.N.

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Authors and Affiliations

Authors

Contributions

D.M.N. and J.A.F. designed the study, performed the research, analysed the data and wrote the paper.

Corresponding author

Correspondence to Jed A. Fuhrman.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–12, Table 1, References and Definitions. (PDF 3783 kb)

Supplementary Data Set 1

Full OTU IDs, taxonomic descriptions and abbreviations. (XLSX 2763 kb)

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Needham, D., Fuhrman, J. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat Microbiol 1, 16005 (2016). https://doi.org/10.1038/nmicrobiol.2016.5

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