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Evolutionary tradeoffs in cellular composition across diverse bacteria

Kempes, Christopher P. and Wang, Lawrence and Amend, Jan P. and Doyle, John and Hoehler, Tori (2016) Evolutionary tradeoffs in cellular composition across diverse bacteria. ISME Journal, 10 (9). pp. 2145-2157. ISSN 1751-7362. http://resolver.caltech.edu/CaltechAUTHORS:20161117-075517086

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Abstract

One of the most important classic and contemporary interests in biology is the connection between cellular composition and physiological function. Decades of research have allowed us to understand the detailed relationship between various cellular components and processes for individual species, and have uncovered common functionality across diverse species. However, there still remains the need for frameworks that can mechanistically predict the tradeoffs between cellular functions and elucidate and interpret average trends across species. Here we provide a comprehensive analysis of how cellular composition changes across the diversity of bacteria as connected with physiological function and metabolism, spanning five orders of magnitude in body size. We present an analysis of the trends with cell volume that covers shifts in genomic, protein, cellular envelope, RNA and ribosomal content. We show that trends in protein content are more complex than a simple proportionality with the overall genome size, and that the number of ribosomes is simply explained by cross-species shifts in biosynthesis requirements. Furthermore, we show that the largest and smallest bacteria are limited by physical space requirements. At the lower end of size, cell volume is dominated by DNA and protein content—the requirement for which predicts a lower limit on cell size that is in good agreement with the smallest observed bacteria. At the upper end of bacterial size, we have identified a point at which the number of ribosomes required for biosynthesis exceeds available cell volume. Between these limits we are able to discuss systematic and dramatic shifts in cellular composition. Much of our analysis is connected with the basic energetics of cells where we show that the scaling of metabolic rate is surprisingly superlinear with all cellular components.


Item Type:Article
Related URLs:
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http://dx.doi.org/10.1038/ismej.2016.21DOIArticle
http://www.nature.com/ismej/journal/v10/n9/full/ismej201621a.htmlPublisherArticle
http://www.nature.com/ismej/journal/v10/n9/suppinfo/ismej201621s1.html?url=/ismej/journal/v10/n9/full/ismej201621a.htmlPublisherSupplementary Information
Additional Information:© 2016 International Society for Microbial Ecology. This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/4.0/. Received 17 August 2015; revised 11 January 2016; accepted 16 January 2016; published online 5 April 2016. CPK acknowledges the support of the ‘Life Underground’ NASA Astrobiology Institute (NNA13AA92A) and the Gordon and Betty Moore Foundation. The authors declare no conflict of interest.
Funders:
Funding AgencyGrant Number
NASANNA13AA92A
Gordon and Betty Moore FoundationUNSPECIFIED
Record Number:CaltechAUTHORS:20161117-075517086
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20161117-075517086
Official Citation:Evolutionary tradeoffs in cellular composition across diverse bacteria Christopher P Kempes, Lawrence Wang, Jan P Amend, John Doyle and Tori Hoehler The ISME Journal (2016) 10, 2145–2157; doi:10.1038/ismej.2016.21
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:72092
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:17 Nov 2016 17:51
Last Modified:17 Nov 2016 17:51

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