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Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean

Nature Microbiology volume 4, pages 1706–1715 (2019)Cite this article

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Abstract

In the surface ocean, phytoplankton transform inorganic substrates into organic matter that fuels the activity of heterotrophic microorganisms, creating intricate metabolic networks that determine the extent of carbon recycling and storage in the ocean. Yet, the diversity of organic molecules and interacting organisms has hindered detection of specific relationships that mediate this large flux of energy and matter. Here, we show that a tightly coupled microbial network based on organic sulfur compounds (sulfonates) exists among key lineages of eukaryotic phytoplankton producers and heterotrophic bacterial consumers in the North Pacific Subtropical Gyre. We find that cultured eukaryotic phytoplankton taxa produce sulfonates, often at millimolar internal concentrations. These same phytoplankton-derived sulfonates support growth requirements of an open-ocean isolate of the SAR11 clade, the most abundant group of marine heterotrophic bacteria. Expression of putative sulfonate biosynthesis genes and sulfonate abundances in natural plankton communities over the diel cycle link sulfonate production to light availability. Contemporaneous expression of sulfonate catabolism genes in heterotrophic bacteria highlights active cycling of sulfonates in situ. Our study provides evidence that sulfonates serve as an ecologically important currency for nutrient and energy exchange between microbial autotrophs and heterotrophs, highlighting the importance of organic sulfur compounds in regulating ecosystem function.

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Fig. 1: Predicted C2-sulfonate and C3-sulfonate biosynthesis routes in eukaryotic phytoplankton.
Fig. 2: Daily sulfonate dynamics over a 4-d period in the North Pacific Subtropical Gyre.
Fig. 3: C2-sulfonate and C3-sulfonate catabolism by heterotrophic bacteria in the North Pacific Subtropical Gyre.

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Data availability

KM1513 cruise information and associated data for the HOE Legacy II cruise can be found online at http://hahana.soest.hawaii.edu/hoelegacy/hoelegacy.html. Raw sequence data for the diel eukaryotic metatranscriptomes are available in the NCBI Sequence Read Archive under BioProject ID PRJNA492142. Raw sequence data for the prokaryotic metatranscriptomes are available under BioProject ID PRJNA492143. Metabolomics data are available in Metabolomics Workbench under project ID PR000797.

Code availability

The custom code used is available on GitHub at https://github.com/IngallsLabUW and https://github.com/armbrustlab.

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Acknowledgements

The data sets presented here resulted from the contributions of many scientists. We acknowledge laboratory assistance from M. Schatz, R. Boccamazzo, G. Workman, N. Kellogg, A. Weid and R. Lionheart. Cultures were kindly provided by R. Cattolico, S. Chisholm, A. Coe, C. Deodato, M. Moran and M. Saito. Assistance with untargeted metabolomics data analysis was generously provided by R. Boiteau. We also thank J. Becker, J. Collins, F. Ribalet, J. Saunders, M. Moran and S. Amin for helpful discussion and feedback. We thank the crew members of the R/V Kilo Moana and S. Wilson for cruise leadership (KM1513), the crew members of the R/V Ka’imikai-O-Kanaloa (KOK1606) and the operational staff of the Simons Collaboration on Ocean Processes and Ecology (SCOPE). This work was supported by grants from the National Science Foundation (Award ID OCE PRF-1521564 to B.P.D. and Award ID OCE-1558483 to R.M.M. and A.E.I.), the Simons Foundation (SCOPE Award ID 329108 to E.V.A. and A.E.I., SF Award ID 385428 to A.E.I. and SF Award ID 426570 to E.V.A.) and the Gordon and Betty Moore Foundation (GBMF3776 to E.V.A.).

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Authors and Affiliations

  1. School of Oceanography, University of Washington, Seattle, WA, USA

    Bryndan P. Durham, Angela K. Boysen, Laura T. Carlson, Ryan D. Groussman, Katherine R. Heal, Kelsy R. Cain, Rhonda L. Morales, Sacha N. Coesel, Robert M. Morris, Anitra E. Ingalls & E. Virginia Armbrust

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  1. Bryndan P. Durham
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Contributions

B.P.D., R.M.M., A.E.I. and E.V.A. designed the study. B.P.D., A.K.B., L.T.C. and K.R.H. generated and analysed the metabolomics data. B.P.D., R.D.G., R.L.M. and S.N.C. generated and analysed the metatranscriptomics data. K.R.C. and R.M.M. performed the SAR11 culture experiments. B.P.D., R.M.M., A.E.I. and E.V.A. wrote the manuscript with contributions from all authors.

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Correspondence to Bryndan P. Durham.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–5, Supplementary Table 1, Supplementary Table 6, Supplementary Table 9, Supplementary Table 11 and Supplementary References.

Reporting Summary

Supplementary Table 2

Measurements of cell count, biomass, and sulfonate concentration for cultures used in metabolomics measurements presented in Table 1.

Supplementary Table 3

Relative abundance of DHPS and DMSP in Thalassiosira pseudonana cells during exponential growth at 10 ppt and 35 ppt in artificial seawater medium.

Supplementary Table 4

Homologs for sulfonate metabolism genes in publicly available phytoplankton genomes at JGI and NCBI.

Supplementary Table 5

Transcript abundances in phytoplankton groups over the course of the diel study in the North Pacific Subtropical Gyre and FDR values from RAIN statistical analysis.

Supplementary Table 7

Sulfonate abundances in seawater plankton over the course of the diel study in the North Pacific Subtropical Gyre.

Supplementary Table 8

Sulfur-containing mass features detected in untargeted liquid chromatography mass spectrometry-based metabolomics data (processed using XCMS) collected near Station ALOHA in the North Pacific Subtropical Gyre.

Supplementary Table 10

Gene homologues for sulfonate catabolism genes present in publically available marine bacterial genomes available through Roseobase (http://www.roseobase.org) and IMG-ER (https://img.jgi.doe.gov/).

Supplementary Table 12

Statistics for ANOVA and Tukey’s honest significance testsc for the SAR11 growth experiments.

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Durham, B.P., Boysen, A.K., Carlson, L.T. et al. Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean. Nat Microbiol 4, 1706–1715 (2019). https://doi.org/10.1038/s41564-019-0507-5

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