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Teamwork in the viscous oceanic microscale

Kanso, Eva A. and Lopes, Rubens M. and Strickler, J. Rudi and Dabiri, John O. and Costello, John H. (2021) Teamwork in the viscous oceanic microscale. Proceedings of the National Academy of Sciences of the United States of America, 118 (29). Art. No. e2018193118. ISSN 0027-8424. PMCID PMC8307612. doi:10.1073/pnas.2018193118. https://resolver.caltech.edu/CaltechAUTHORS:20210719-172443474

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[img] Video (QuickTime) (Movie_S01. Streak flows around Coscinodiscus wailesii diatom host with multiple attached Pseudovorticella coscinodisci ciliate epibionts) - Supplemental Material
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[img] Video (QuickTime) (Movie S2. Flows around Coscinodiscus wailesii diatom host with an attached Pseudovorticella coscinodisci ciliate epibiont.) - Supplemental Material
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[img] Video (QuickTime) (Movie S3. Flow streak lines around Coscinodiscus wailesii diatom host with an attached Pseudovorticella coscinodisci ciliate epibiont. Streak lines were derived from the image sequence of Movie 2 by integrating particle paths over 200 frame intervals) - Supplemental Material
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[img] Video (QuickTime) (Movie S4. Flow generated by multiple Pseudovorticella coscinodisci ciliate epibionts on a 350 μm diameter Coscinodiscus wailesii diatom host with playback at real time. Images captured and played at 125 fps) - Supplemental Material
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[img] Video (QuickTime) (Movie S5. Rotation of Coscinodiscus wailesii diatom host with multiple attached Pseudovorticella coscinodisci ciliate epibionts. Unbalanced forces generated by ciliates result in rotational motion of consortia) - Supplemental Material
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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2018193118DOIArticle
https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2018193118/-/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8307612PubMed CentralArticle
ORCID:
AuthorORCID
Kanso, Eva A.0000-0003-0336-585X
Lopes, Rubens M.0000-0002-9709-073X
Strickler, J. Rudi0000-0003-1183-2710
Dabiri, John O.0000-0002-6722-9008
Costello, John H.0000-0002-6967-3145
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.
Group:GALCIT
Funders:
Funding AgencyGrant Number
NSFCBET-2100209
NSFCMMI-2034043
NIHR01 HL 153622-01A1
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)310642/2017-5
NSFOCE-2100705
Subject Keywords:phytoplankton | nutrient limitation | symbiosis | diffusion limitation | cell size
Issue or Number:29
PubMed Central ID:PMC8307612
DOI:10.1073/pnas.2018193118
Record Number:CaltechAUTHORS:20210719-172443474
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210719-172443474
Official Citation:Teamwork in the viscous oceanic microscale Eva A. Kanso, Rubens M. Lopes, J. Rudi Strickler, John O. Dabiri, John H. Costello Proceedings of the National Academy of Sciences Jul 2021, 118 (29) e2018193118; DOI: 10.1073/pnas.2018193118
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109911
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:19 Jul 2021 20:55
Last Modified:02 Aug 2021 16:19

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