Letter

Surface properties of SAR11 bacteria facilitate grazing avoidance

Received:
Accepted:
Published online:

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.

  • Subscribe to Nature Microbiology for full access:

    $59

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

Change history

  • Correction 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.

References

  1. 1.

    Worden, A. Z. et al. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microorganisms. Science 347, 1257594 (2015).

  2. 2.

    Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007).

  3. 3.

    Kirchman, D. L. Microbial Ecology of the Oceans. (WileyLiss, New York, 2008).

  4. 4.

    Teeling, H. et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611 (2012).

  5. 5.

    Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002).

  6. 6.

    Eiler, A., Hayakawa, D. H., Church, M. J., Karl, D. M. & Rappé, M. S. Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre. Environ. Microbiol. 11, 2291–2300 (2009).

  7. 7.

    Giovannoni, S. J. SAR11 Bacteria: the most abundant plankton in the oceans. Ann. Rev. Mar. Sci. 9, 1–25 (2016).

  8. 8.

    Rappé, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, S. J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002).

  9. 9.

    Zhao, Y. et al. Abundant SAR11 viruses in the ocean. Nature 494, 357–360 (2013).

  10. 10.

    Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol. 3, 537–546 (2005).

  11. 11.

    Suzuki, M. T. Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat. Microb. Ecol. 20, 261–272 (1999).

  12. 12.

    Matz, C. & Kjelleberg, S. Off the hook – how bacteria survive protozoan grazing. Trends Microbiol. 13, 302–307 (2005).

  13. 13.

    Petersen, J. K. Ascidian suspension feeding. J. Exp. Mar. Bio. Ecol. 342, 127–137 (2007).

  14. 14.

    Morganti, T. M., Yahel, G., Ribes, M. & Coma, R. ‘VacuSIP’, an improved InEx method for in situ measurement of particulate and dissolved compounds processed by active suspension feeders. J. Vis. Exp. 114, e54221 (2016).

  15. 15.

    Mary, I. et al. SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquat. Microb. Ecol. 45, 107–113 (2006).

  16. 16.

    Chesson, J. The estimation and analysis of preference and its relatioship to foraging models. Ecology 64, 1297–1304 (1983).

  17. 17.

    Yahel, G., Marie, D., Beninger, P., Eckstein, S. & Genin, A. In situ evidence for pre-capture qualitative selection in the tropical bivalve Lithophaga simplex. Aquat. Biol. 6, 235–246 (2009).

  18. 18.

    Yahel, G., Eerkes-Medrano, D. & Leys, S. Size independent selective filtration of ultraplankton by hexactinellid glass sponges. Aquat. Microb. Ecol. 45, 181–194 (2006).

  19. 19.

    De Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1–12 (2015).

  20. 20.

    Scheinberg, R. D., Landry, M. R. & Calbet, A. Grazing of two common appendicularians on the natural prey assemblage of a tropical coastal ecosystem. Mar. Ecol. Prog. Ser. 294, 201–212 (2005).

  21. 21.

    Alldredge, A. L. The impact of appendicularian grazing on natural food concentrations in situ. Limnol. Oceanogr. 26, 247–257 (1981).

  22. 22.

    D’Alelio, D., Libralato, S., Wyatt, T. & Ribera d’Alcalà, M. Ecological-network models link diversity, structure and function in the plankton food-web. Sci. Rep. 6, 21806 (2016).

  23. 23.

    Flood, P. R. Architecture of, and water circulation and flow rate in, the house of the planktonic tunicate Oikopleura labradoriensis. Mar. Biol. 111, 95–111 (1991).

  24. 24.

    Robison, B. H., Reisenbichler, K. R. & Sherlock, R. E. Giant larvacean houses: rapid carbon transport to the deep sea floor. Science 308, 1609–1611 (2005).

  25. 25.

    Shimeta, J. & Jumars, P. A. Physical mechanisms and rates of particle capture by suspension feeders. Oceanogr. Mar. Biol. Annu. Rev. 29, 191–257 (1991).

  26. 26.

    Guieb, R. A., Jumars, P. A. & Self, R. F. L. Adhesive-based selection by a tentacle-feeding polychaete for particle size, shape and bacterial coating in silt and sand. J. Mar. Res. 62, 260–281 (2004).

  27. 27.

    Busscher, H. J. & Weerkamp, A. H. Specific and non-specific interactions in bacterial adhesion to solid substrata. FEMS Microbiol. Lett. 46, 165–173 (1987).

  28. 28.

    Monger, B. C., Landry, M. R. & Brown, S. L. Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol. Oceanogr. 44, 1917–1927 (1999).

  29. 29.

    Tarao, M., Jezbera, J. & Hahn, M. W. Involvement of cell surface structures in size-independent grazing resistance of freshwater Actinobacteria. Appl. Environ. Microbiol. 75, 4720–4726 (2009).

  30. 30.

    Yawata, Y. et al. Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations. Proc. Natl Acad. Sci. USA 111, 5622–5627 (2014).

  31. 31.

    Lai, S. K., Wang, Y. Y., Wirtz, D. & Hanes, J. Micro- and macrorheology of mucus. Adv. Drug Deliv. Rev. 61, 86–100 (2010).

  32. 32.

    Riisgård, H. U. On measurement of filtration rates in bivalves — the stony road to reliable data: review and interpretation. Mar. Ecol. Prog. Ser. 211, 275–291 (2001).

  33. 33.

    Marie, D., Brussaard, C., Thyrhaug, R., Bratbak, G. & Vaulot, D. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ. Microbiol. 65, 45–52 (1999).

  34. 34.

    Simon, N., Barlow, G. R., Marie, D., Partensky, F. & Vaulot, D. Characterization of oceanic photosynthetic picoeukaryotes by flow cytometery. J. Phycol. 30, 922–935 (1994).

  35. 35.

    Cunningham, A. & Buonnacorsi, G. A. Narrow-angle forward light scattering from individual algal cells: Implications for size and shape discrimination in flow cytometry. J. Plankton Res. 14, 223–234 (1992).

  36. 36.

    Robertson, B. & Button, D. Characterizing aquatic bacteria according to population, cell size, and apparent. DNA content by flow cytometry. Cytometry 10, 70–76 (1989).

  37. 37.

    Pruesse, E., Peplies, J. & Glöckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829 (2012).

  38. 38.

    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).

  39. 39.

    Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

  40. 40.

    Camacho, C. et al. BLAST plus: architecture and applications. BMC Bioinformatics 10, 421 (2009).

  41. 41.

    Suzuki, M. T., Béjà, O., Taylor, L. T. & Delong, E. F. Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environ. Microbiol. 3, 323–331 (2001).

  42. 42.

    Morris, R. M. et al. Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnol. Oceanogr. 50, 1687–1696 (2005).

  43. 43.

    Carlson, C. A. et al. Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J. 3, 283–295 (2009).

  44. 44.

    Brown, M. V. et al. Global biogeography of SAR11 marine bacteria. Mol. Syst. Biol. 8, 59 (2012).

  45. 45.

    Vergin, K. L. et al. High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J. 7, 1332–1332 (2013).

  46. 46.

    Ondov, B. D., Bergman, N. H. & Phillippy, A. M. Interactive metagenomic visualization in a web browser. BMC Bioinformatics 12, 385 (2011).

  47. 47.

    Pernthaler, A., Pernthaler, J. & Amann, R. Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria. Appl. Environ. Microbiol. 68, 3094–3101 (2002).

  48. 48.

    Pernthaler, A., Pernthaler, J. & Amann, R. in Molecular Microbial Ecology Manual (eds Kowalchuk, G. A., de Bruijn, F., Head, I. M., Van der Zijpp, A. J. & J. D. van Elsa) 711–725 (Springer, Netherlands, 2004).

  49. 49.

    Amann, R. I., Krumholz, L. & Stahl, D. A. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol. 172, 762–770 (1990).

  50. 50.

    Amann, R. I., Ludwig, W. & Schleifer, K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143–69 (1995).

  51. 51.

    Stingl, U., Tripp, H. J. & Giovannoni, S. J. Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time-series Study site. ISME J. 1, 361–371 (2007).

  52. 52.

    Carini, P., Steindler, L., Beszteri, S. & Giovannoni, S. J. Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium. ISME J. 7, 592–602 (2013).

  53. 53.

    Guillard, R. & Hargraves, P. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32, 234–236 (1993).

  54. 54.

    Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

  55. 55.

    Toribio, A. L. et al. European nucleotide archive in 2016. Nucleic Acids Res. 45, D32–D36 (2017).

  56. 56.

    Yilmaz, P. et al. Minimum information about a marker gene sequence (MIMARKS) and minimum information about any (x) sequence (MIxS) specifications. Nat. Biotechnol. 29, 415–420 (2011).

  57. 57.

    Diepenbroek, M. et al. in: Informatik 2014 – Big Data Komplexität meistern (eds Plödereder, E., Grunske, L., Schneider, E. & Ull, D.) 1711–1724 (Köllen Verlag, Bonn, 2014).

Download references

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.

Author information

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

Authors

  1. Search for Ayelet Dadon-Pilosof in:

  2. Search for Keats R. Conley in:

  3. Search for Yuval Jacobi in:

  4. Search for Markus Haber in:

  5. Search for Fabien Lombard in:

  6. Search for Kelly R. Sutherland in:

  7. Search for Laura Steindler in:

  8. Search for Yaron Tikochinski in:

  9. Search for Michael Richter in:

  10. Search for Frank Oliver Glöckner in:

  11. Search for Marcelino T. Suzuki in:

  12. Search for Nyree J. West in:

  13. Search for Amatzia Genin in:

  14. Search for Gitai Yahel in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Ayelet Dadon-Pilosof.

Electronic supplementary material