Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations

Although competition–dispersal tradeoffs are commonly invoked to explain species coexistence for animals and plants in spatially structured environments, such mechanisms for coexistence remain unknown for microorganisms. Here we show that two recently speciated marine bacterioplankton populations pu...

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Main Authors: Yawata, Yutaka, Menolascina, Filippo, Hehemann, Jan-Hendrik, Stocker, Roman, Cordero Sanchez, Otto X., Polz, Martin F
Other Authors: Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Format: Article
Language:en_US
Published: National Academy of Sciences (U.S.) 2014
Online Access:http://hdl.handle.net/1721.1/91515
https://orcid.org/0000-0002-3370-6080
https://orcid.org/0000-0001-9296-3733
https://orcid.org/0000-0002-4937-7912
https://orcid.org/0000-0002-3199-0508
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author Yawata, Yutaka
Menolascina, Filippo
Hehemann, Jan-Hendrik
Stocker, Roman
Cordero Sanchez, Otto X.
Polz, Martin F
author2 Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
author_facet Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Yawata, Yutaka
Menolascina, Filippo
Hehemann, Jan-Hendrik
Stocker, Roman
Cordero Sanchez, Otto X.
Polz, Martin F
author_sort Yawata, Yutaka
collection MIT
description Although competition–dispersal tradeoffs are commonly invoked to explain species coexistence for animals and plants in spatially structured environments, such mechanisms for coexistence remain unknown for microorganisms. Here we show that two recently speciated marine bacterioplankton populations pursue different behavioral strategies to exploit nutrient particles in adaptation to the landscape of ephemeral nutrient patches characteristic of ocean water. These differences are mediated primarily by differential colonization of and dispersal among particles. Whereas one population is specialized to colonize particles by attaching and growing biofilms, the other is specialized to disperse among particles by rapidly detecting and swimming toward new particles, implying that it can better exploit short-lived patches. Because the two populations are very similar in their genomic composition, metabolic abilities, chemotactic sensitivity, and swimming speed, this fine-scale behavioral adaptation may have been responsible for the onset of the ecological differentiation between them. These results demonstrate that the principles of spatial ecology, traditionally applied at macroscales, can be extended to the ocean’s microscale to understand how the rich spatiotemporal structure of the resource landscape contributes to the fine-scale ecological differentiation and species coexistence among marine bacteria.
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spelling mit-1721.1/915152022-09-30T07:38:14Z Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations Yawata, Yutaka Menolascina, Filippo Hehemann, Jan-Hendrik Stocker, Roman Cordero Sanchez, Otto X. Polz, Martin F Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Parsons Laboratory for Environmental Science and Engineering (Massachusetts Institute of Technology) Yawata, Yutaka Cordero Sanchez, Otto Xavier Menolascina, Filippo Hehemann, Jan-Hendrik Polz, Martin F. Stocker, Roman Although competition–dispersal tradeoffs are commonly invoked to explain species coexistence for animals and plants in spatially structured environments, such mechanisms for coexistence remain unknown for microorganisms. Here we show that two recently speciated marine bacterioplankton populations pursue different behavioral strategies to exploit nutrient particles in adaptation to the landscape of ephemeral nutrient patches characteristic of ocean water. These differences are mediated primarily by differential colonization of and dispersal among particles. Whereas one population is specialized to colonize particles by attaching and growing biofilms, the other is specialized to disperse among particles by rapidly detecting and swimming toward new particles, implying that it can better exploit short-lived patches. Because the two populations are very similar in their genomic composition, metabolic abilities, chemotactic sensitivity, and swimming speed, this fine-scale behavioral adaptation may have been responsible for the onset of the ecological differentiation between them. These results demonstrate that the principles of spatial ecology, traditionally applied at macroscales, can be extended to the ocean’s microscale to understand how the rich spatiotemporal structure of the resource landscape contributes to the fine-scale ecological differentiation and species coexistence among marine bacteria. Japan Society for the Promotion of Science National Science Foundation (U.S.) (Grant OCE-0744641-CAREER) Gordon and Betty Moore Foundation (Microbial Initiative Investigator Award 3783) National Institutes of Health (U.S.) (Grant 1R01GM100473-01) 2014-11-10T14:52:32Z 2014-11-10T14:52:32Z 2014-04 2013-10 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/91515 Yawata, Y., O. X. Cordero, F. Menolascina, J.-H. Hehemann, M. F. Polz, and R. Stocker. “Competition-Dispersal Tradeoff Ecologically Differentiates Recently Speciated Marine Bacterioplankton Populations.” Proceedings of the National Academy of Sciences 111.15 (2014): 5622–5627. https://orcid.org/0000-0002-3370-6080 https://orcid.org/0000-0001-9296-3733 https://orcid.org/0000-0002-4937-7912 https://orcid.org/0000-0002-3199-0508 en_US http://dx.doi.org/10.1073/pnas.1318943111 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS
spellingShingle Yawata, Yutaka
Menolascina, Filippo
Hehemann, Jan-Hendrik
Stocker, Roman
Cordero Sanchez, Otto X.
Polz, Martin F
Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
title Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
title_full Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
title_fullStr Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
title_full_unstemmed Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
title_short Competition-dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
title_sort competition dispersal tradeoff ecologically differentiates recently speciated marine bacterioplankton populations
url http://hdl.handle.net/1721.1/91515
https://orcid.org/0000-0002-3370-6080
https://orcid.org/0000-0001-9296-3733
https://orcid.org/0000-0002-4937-7912
https://orcid.org/0000-0002-3199-0508
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