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Surface properties of SAR11 bacteria facilitate grazing avoidance

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

This article has been updated

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.

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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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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