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SAR11 marine bacteria require exogenous reduced sulphur for growth

Nature volume 452, pages 741–744 (2008)Cite this article

Abstract

Sulphur is a universally required cell nutrient found in two amino acids and other small organic molecules. All aerobic marine bacteria are known to use assimilatory sulphate reduction to supply sulphur for biosynthesis, although many can assimilate sulphur from organic compounds that contain reduced sulphur atoms1,2,3. An analysis of three complete ‘Candidatus Pelagibacter ubique’ genomes, and public ocean metagenomic data sets, suggested that members of the ubiquitous and abundant SAR11 alphaproteobacterial clade are deficient in assimilatory sulphate reduction genes. Here we show that SAR11 requires exogenous sources of reduced sulphur, such as methionine or 3-dimethylsulphoniopropionate (DMSP) for growth. Titrations of the algal osmolyte DMSP in seawater medium containing all other macronutrients in excess showed that 1.5 × 108 SAR11 cells are produced per nanomole of DMSP. Although it has been shown that other marine alphaproteobacteria use sulphur from DMSP in preference to sulphate1,2, our results indicate that ‘Cand. P. ubique’ relies exclusively on reduced sulphur compounds that originate from other plankton.

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Figure 1: Sulphur metabolism pathways and comparative genomics.
Figure 2: 35 S radiotracer uptake and growth responses to additions of sulphur compounds.
Figure 3: Growth curves for 21-nM additions of various reduced sulphur sources.

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Acknowledgements

We thank U. Stingl, C. Carlson and A. Treusch for discussions, R. Kiene for 35S[DMSP], and K. Vergin for assistance with radiotracers. This work was supported by grants from the Marine Microbiology Initiative of the Gordon and Betty Moore Foundation and the National Science Foundation.

Author Contributions H.J.T. conducted genome analysis, adaptation of Guava EasyCyte to marine picoplankton counting, initial experimental design, preliminary data collection and analysis, and wrote the manuscript. J.B.K. set up, performed, and collected data for many culture experiments, and assisted in EasyCyte adaptations. J.W.H.D. provided DMSP and DMSP measurements. L.J.W. performed metagenomics. S.J.G. initiated the study, suggested candidate nutrients for testing, and with M.S.S. suggested final experiments and data presentation. All authors reviewed the manuscript before submission.

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Authors and Affiliations

  1. Department of Microbiology, 220 Nash Hall, Oregon State University, Corvallis, Oregon 97331, USA,

    H. James Tripp, Joshua B. Kitner, Michael S. Schwalbach, Larry J. Wilhelm & Stephen J. Giovannoni

  2. Woods Hole Oceanographic Institution, Redfield 3-22, MS no. 32, Woods Hole, Massachusetts 02543, USA,

    John W. H. Dacey

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  1. H. James Tripp
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Correspondence to Stephen J. Giovannoni.

Supplementary information

Supplementary Information

The file contains Supplementary Methods, Supplementary Notes, Supplementary Figures 1-4 with Legends and Supplementary Table 1 with Legend. The Supplementary Methods describe the search for sulphate reduction genes. The Supplementary Notes describe cell size and morphology, identify putative genes and metabolic pathways for sulphur metabolism, and demonstrate the infeasibility of 35SO4 uptake experiments, other sources of reduced sulfur in the oceanic water column, and consistency of cell morphology and size. The Supplementary Figures and Tables are included within the notes. (PDF 195 kb)

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Tripp, H., Kitner, J., Schwalbach, M. et al. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452, 741–744 (2008). https://doi.org/10.1038/nature06776

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