Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Healthy herds in the phytoplankton: the benefit of selective parasitism

Abstract

The impact of selective predation of weaker individuals on the general health of prey populations is well-established in animal ecology. Analogous processes have not been considered at microbial scales despite the ubiquity of microbe-microbe interactions, such as parasitism. Here we present insights into the biotic interactions between a widespread marine thraustochytrid and a diatom from the ecologically important genus Chaetoceros. Physiological experiments show the thraustochytrid targets senescent diatom cells in a similar way to selective animal predation on weaker prey individuals. This physiology-selective targeting of ‘unhealthy’ cells appears to improve the overall health (i.e., increased photosynthetic quantum yield) of the diatom population without impacting density, providing support for ‘healthy herd’ dynamics in a protist–protist interaction, a phenomenon typically associated with animal predators and their prey. Thus, our study suggests caution against the assumption that protist–protist parasitism is always detrimental to the host population and highlights the complexity of microbial interactions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Growth experiments demonstrate that thraustochytrids preferentially target and grow on unhealthy diatom cells.
Fig. 2: Selective targeting of unhealthy diatom cells by thraustochytrids improves the overall health of the diatom population.

References

  1. 1.

    Slobodkin LB. Prudent predation does not require group selection. Am Nat. 1974;108:665–78.

    Article  Google Scholar 

  2. 2.

    Williams PD. Unhealthy herds: some epidemiological consequences of host heterogeneity in predator-host-parasite systems. J Theor Biol. 2008;253:500–7.

    Article  Google Scholar 

  3. 3.

    Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP. Keeping the herds healthy and alert: Implications of predator control for infectious disease. Ecol Lett. 2003;6:797–802.

    Article  Google Scholar 

  4. 4.

    Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, et al. Determinants of community structure in the global plankton interactome. Science 2015;348:1262073.

    Article  Google Scholar 

  5. 5.

    Skovgaard A. Dirty tricks in the plankton: Diversity and role of marine parasitic protists. Acta Protozool. 2014;53:51–62.

    Google Scholar 

  6. 6.

    Jephcott TG, Sime-Ngando T, Gleason FH, Macarthur DJ. Host-parasite interactions in food webs: Diversity, stability, and coevolution. Food Webs. 2016;6:1–8.

    Article  Google Scholar 

  7. 7.

    Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B. Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cycles. 1995;9:359–72.

    CAS  Article  Google Scholar 

  8. 8.

    Timmermans KR, Veldhuis MJ, Brussaard CP. Cell death in three marine diatom species in response to different irradiance levels, silicate, or iron concentrations. Aquat Micro Ecol. 2007;46:253–61.

    Article  Google Scholar 

  9. 9.

    Pinto E, Van Nieuwerburgh L, De Barros MP, Pedersén M, Colepicolo P, Snoeijs P. Density-dependent patterns of thiamine and pigment production in the diatom Nitzschia microcephala. Phytochemistry. 2003;63:155–63.

    CAS  Article  Google Scholar 

  10. 10.

    Manoylov KM. Intra- and interspecific competition for nutrients and light in diatom cultures. J Freshw Ecol. 2009;24:145–57.

    Article  Google Scholar 

  11. 11.

    Houston DC, Cooper JE. The digestive tract of the whiteback griffon vulture and its role in disease transmission among wild ungulates. J Wildl Dis. 1975;11:306–13.

    CAS  Article  Google Scholar 

  12. 12.

    Schaller G. The Serengeti lion: a study of predator-prey relations. London: University of Chicago Press; 1972.

  13. 13.

    Krumm CE, Conner MM, Hobbs NT, Hunter DO, Miller MW. Mountain lions prey selectively on prion-infected mule deer. Biol Lett. 2010;6:209–11.

    Article  Google Scholar 

  14. 14.

    Pole A, Gordon IJ, Gorman ML, MacAskill M. Prey selection by African wild dogs (Lycaon pictus) in southern Zimbabwe. J Zool. 2004;262:207–15.

    Article  Google Scholar 

  15. 15.

    Husseman JS, Murray DL, Power G, Mack C, Wenger CR, Quigley H. Assessing differential prey selection patterns between two sympatric large carnivores. Oikos. 2003;101:591–601.

    Article  Google Scholar 

  16. 16.

    Lafferty KD. Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol Appl. 2004;14:1566–73.

    Article  Google Scholar 

  17. 17.

    Duffy MA, Hall SR, Tessier AJ, Huebner M. Selective predators and their parasitized prey: Are epidemics in zooplankton under top-down control? Limnol Oceanogr. 2005;50:412–20.

    Article  Google Scholar 

  18. 18.

    Hudson PJ, Dobson AP, Newborn D. Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol. 1992;61:681.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the crew of the RV Sepia for sampling and Angela Ward and Claire Hopkins (MBA) for their guidance with isolation and culturing. We also thank Glenn Harper, Alex Strachan and the team at the Plymouth Electron Microscopy Centre (PEMC) for their assistance with SEM. We are indebted to Jingwen Pan (University of British Columbia) and Javier del Campo (Institute of Evolutionary Biology, Spain) for providing the reference sequences used in building phylogenetic trees in this study, as well as to Daniel Vaulot (Station Biologique de Roscoff) for help in interpreting the Ocean Sampling Day data. Nathan Chrismas (MBA) is also thanked for bioinformatic support.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Michael Cunliffe.

Ethics declarations

Conflict of interest

The author declares no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Laundon, D., Mock, T., Wheeler, G. et al. Healthy herds in the phytoplankton: the benefit of selective parasitism. ISME J 15, 2163–2166 (2021). https://doi.org/10.1038/s41396-021-00936-8

Download citation

Search

Quick links