Teamwork in the viscous oceanic microscale

Creators: Kanso, Eva A.; Lopes, Rubens M.; Strickler, J. Rudi; Dabiri, John O.; Costello, John H.

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Abstract

Nutrient acquisition is crucial for oceanic microbes, and competitive solutions to solve this challenge have evolved among a range of unicellular protists. However, solitary solutions are not the only approach found in natural populations. A diverse array of oceanic protists form temporary or even long-lasting attachments to other protists and marine aggregates. Do these planktonic consortia provide benefits to their members? Here, we use empirical and modeling approaches to evaluate whether the relationship between a large centric diatom, Coscinodiscus wailesii, and a ciliate epibiont, Pseudovorticella coscinodisci, provides nutrient flux benefits to the host diatom. We find that fluid flows generated by ciliary beating can increase nutrient flux to a diatom cell surface four to 10 times that of a still cell without ciliate epibionts. This cosmopolitan species of diatom does not form consortia in all environments but frequently joins such consortia in nutrient-depleted waters. Our results demonstrate that symbiotic consortia provide a cooperative alternative of comparable or greater magnitude to sinking for enhancement of nutrient acquisition in challenging environments.

Additional Information

© 2021 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by David M. Karl, University of Hawai'i at Mãnoa, Honolulu, HI, and approved June 1, 2021 (received for review August 27, 2020). We are grateful to Y. Garcia for help with organism sampling and sorting. E.A.K. is funded by NSF-2100209, NSF RAISE IOS-2034043 and NIH R01 HL 153622-01A1. R.M.L. is a CNPq research fellow (grant # 310642/2017-5). J.H.C. and J.O.D. are funded by Grant NSF-2100705. Author contributions: R.M.L., J.R.S., and J.H.C. designed research; R.M.L., J.R.S., and J.H.C. performed research; E.A.K., J.O.D., and J.H.C. contributed new analytic tools; E.A.K., R.M.L., J.R.S., J.O.D., and J.H.C. analyzed data; and E.A.K., R.M.L., and J.H.C. wrote the paper. The authors declare no competing interest. This article is a PNAS Direct Submission. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2018193118/-/DCSupplemental.