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Surface properties of SAR11 bacteria facilitate grazing avoidance

Nature Microbiology volume 2, pages 1608–1615 (2017)Cite this article

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An Author Correction to this article was published on 20 October 2017

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Abstract

Oceanic ecosystems are dominated by minute microorganisms that play a major role in food webs and biogeochemical cycles1. Many microorganisms thrive in the dilute environment due to their capacity to locate, attach to, and use patches of nutrients and organic matter2,3. We propose that some free-living planktonic bacteria have traded their ability to stick to nutrient-rich organic particles for a non-stick cell surface that helps them evade predation by mucous filter feeders. We used a combination of in situ sampling techniques and next-generation sequencing to study the biological filtration of microorganisms at the phylotype level. Our data indicate that some marine bacteria, most notably the highly abundant Pelagibacter ubique and most other members of the SAR 11 clade of the Alphaproteobacteria, can evade filtration by slipping through the mucous nets of both pelagic and benthic tunicates. While 0.3 µm polystyrene beads and other similarly-sized bacteria were efficiently filtered, SAR11 members were not captured. Reversed-phase chromatography revealed that most SAR11 bacteria have a much less hydrophobic cell surface than that of other planktonic bacteria. Our data call for a reconsideration of the role of surface properties in biological filtration and predator-prey interactions in aquatic systems.

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Fig. 1: Differential retention of marine microorganisms by the ascidian Microcosmus exasperatus measured in situ (10 m depth) at the Eastern Mediterranean Sea (n = 15, Michmoret, Central Israel, September 2014).
Fig. 2: Differential clearance rate of marine microorganisms by the appendicularian Oikopleura albicans measured by in situ incubations in the NW Mediterranean Sea during April 2014, n = 15.
Fig. 3: Hydrophobicity of cultures bacteria measured by HIC for four autotrophs, two heterotrophic copiotrophs and five heterotrophic oligotrophic bacterial cultures.
Fig. 4: Hydrophobicity of naturally occurring marine bacteria measured by HIC in surface seawater samples collected at ~10 m depth.

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Change history

  • 20 October 2017

    In the version of this Letter originally published, the authors incorrectly stated that primers 28F-519R were reported in ref. 54 to underestimate the abundance of SAR11 in the ocean. This statement has now been amended in all versions of the Letter.

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Acknowledgements

We thank S. Giovannoni for providing strains HTCC1062, HTCC2506 and HTCC2143, and L. Gomez-Consarnau for providing strains MED134 and DLF12 and D. Roth-Rosenberg and D. Sher lab for providing strain PRO9312. M. Landry for useful discussion and help with HIC application. M. Gilboa and staff of the School of Marine Science, Ruppin for technical assistance. BSF grant 2012089 to K.S, Y.T. and G.Y. ISF grant 1280/13 to G.Y. ECOGELY ANR-10-PDOC-005-01 to F.L. and ANR RHOMEO 11-BSV7-0021 to M.T.S. We thank the Bio2Mar, and Cytometry-Imaging platforms of the OOB and EMBRC-zooplankton of OOV for access to instrumentation. Support provided to A.D.P by the Mediterranean Sea Research Center of Israel and IUI PhD award.

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Authors and Affiliations

  1. The School of Marine Science, Ruppin Academic Center, 4029700, Michmoret, Israel

    Ayelet Dadon-Pilosof, Yuval Jacobi, Yaron Tikochinski & Gitai Yahel

  2. Department of Ecology, Evolution & Behavior, The Hebrew University of Jerusalem, 9190401, Jerusalem, Israel

    Ayelet Dadon-Pilosof & Amatzia Genin

  3. Oregon Institute of Marine Biology, University of Oregon, Eugene, OR, 97403, USA

    Keats R. Conley & Kelly R. Sutherland

  4. School of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, 69978, Tel Aviv, Israel

    Yuval Jacobi

  5. Department of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, 3498838, Haifa, Israel

    Markus Haber & Laura Steindler

  6. Sorbonne Universités, Université Pierre et Marie Curie, Observatoire Océanologique de Villefranche-Sur-Mer (OOV), Laboratoire d’Océanographie de Villefranche-sur-Mer, 06230, Villefranche-sur-Mer, France

    Fabien Lombard

  7. Max Planck Institute for Marine Microbiology Microbial Genomics and Bioinformatics Research Group Celsiusstrasse 1, 28359, Bremen, Germany

    Michael Richter & Frank Oliver Glöckner

  8. Jacobs University, Campusring 1, 28759, Bremen, Germany

    Frank Oliver Glöckner

  9. Sorbonne Universités, UPMC Univ Paris 06, CNRS, Laboratoire de Biodiversité et Biotechnologies Microbiennes (LBBM), Observatoire Océanologique, F-66650, Banyuls-sur-mer, France

    Marcelino T. Suzuki

  10. Sorbonne Universités, UPMC Univ Paris 06, CNRS, Observatoire Océanologique de Banyuls (OOB), F-66650, Banyuls-sur-mer, France

    Nyree J. West

  11. The Interuniversity Institute for Marine Sciences in Eilat, 8810302, Eilat, Israel

    Amatzia Genin

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  1. Ayelet Dadon-Pilosof
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Contributions

A.D.-P. was involved in study design, performed the in situ and lab experiments, fine-tuned protocols, compiled and analyzed FCM, FISH, HIC and sequencing data and prepared the manuscript. G.Y. designed the study, and participated in field experiments, data analysis and manuscript preparation. A.G. was involved in planning the study. Y.T. and L.S. were involved in study design. L.S. and M.H. cultured oligotrophic and copiotrophic bacteria utilized for column experiments. K.R.C., K.S. and F.L. participated in planning some of the experiments, field and lab sampling. N.J.W. and M.T.S. were involved in the FISH experiments and data analysis. M.R. designed and performed bioinformatics analyses F.O.G. designed bioinformatics analyses Y.J. performed beads experiments. All authors discussed the results and commented on the manuscript during its preparation.

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Correspondence to Ayelet Dadon-Pilosof.

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A correction to this article is available online at https://doi.org/10.1038/s41564-017-0064-8.

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Dadon-Pilosof, A., Conley, K.R., Jacobi, Y. et al. Surface properties of SAR11 bacteria facilitate grazing avoidance. Nat Microbiol 2, 1608–1615 (2017). https://doi.org/10.1038/s41564-017-0030-5

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