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Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins

Li, Po-Nan and Herrmann, Jonathan and Tolar, Bradley B. and Poitevin, Frédéric and Ramdasi, Rasika and Bargar, John R. and Stahl, David A. and Jensen, Grant J. and Francis, Christopher A. and Wakatsuki, Soichi and van den Bedem, Henry (2018) Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins. ISME Journal, 12 (10). pp. 2389-2402. ISSN 1751-7362. http://resolver.caltech.edu/CaltechAUTHORS:20180618-091246320

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Abstract

Surface layers (S-layers) are two-dimensional, proteinaceous, porous lattices that form the outermost cell envelope component of virtually all archaea and many bacteria. Despite exceptional sequence diversity, S-layer proteins (SLPs) share important characteristics such as their ability to form crystalline sheets punctuated with nano-scale pores, and their propensity for charged amino acids, leading to acidic or basic isoelectric points. However, the precise function of S-layers, or the role of charged SLPs and how they relate to cellular metabolism is unknown. Nano-scale lattices affect the diffusion behavior of low-concentration solutes, even if they are significantly smaller than the pore size. Here, we offer a rationale for charged S-layer proteins in the context of the structural evolution of S-layers. Using the ammonia-oxidizing archaea (AOA) as a model for S-layer geometry, and a 2D electrodiffusion reaction computational framework to simulate diffusion and consumption of the charged solute ammonium (NH_4^+), we find that the characteristic length scales of nanoporous S-layers elevate the concentration of NH_4^+ in the pseudo-periplasmic space. Our simulations suggest an evolutionary, mechanistic basis for S-layer charge and shed light on the unique ability of some AOA to oxidize ammonia in environments with nanomolar NH_4^+ availability, with broad implications for comparisons of ecologically distinct populations.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41396-018-0191-0DOIArticle
https://rdcu.be/ZuUTPublisherFree ReadCube access
ORCID:
AuthorORCID
Li, Po-Nan0000-0002-7917-7444
Tolar, Bradley B.0000-0003-0493-1470
Jensen, Grant J.0000-0003-1556-4864
van den Bedem, Henry0000-0003-2358-841X
Additional Information:© 2018 International Society for Microbial Ecology. Received: 30 November 2017; Revised: 11 April 2018; Accepted: 14 April 2018; Published online 13 June 2018. This work was partially supported by the US Department of Energy, Laboratory Directed Research and Development under contract No. DE-AC02-76SF00515. JH was supported by the National Science Foundation Graduate Research Fellowship Program (NSF-GRFP), as well as the US Department of Energy Office of Science Graduate Student Research Program (DOE-SCGSR). FP acknowledges support from the National Institutes of Health (NIH), grant No. R35GM122543. DAS was funded in part by the United States National Science Foundation Grants MCB-092074 and OCE-1046017. HvdB acknowledges support from the U.S. Department of Energy, Office of Science, Office of Advanced Scientific Computing Research, Scientific Discovery through Advanced Computing (SciDAC) program. Computations were performed at the Stanford Research Computing Center. Glycosylation analysis by mass spectrometry was possible with assistance from C Adams and R Lieb (Stanford University Mass Spectrometry). The authors declare that they have no conflict of interest.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-AC02-76SF00515
NSF Graduate Research FellowshipUNSPECIFIED
NIHR35GM122543
NSFMCB-0920741
NSFOCE-1046017
Record Number:CaltechAUTHORS:20180618-091246320
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180618-091246320
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:87184
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:18 Jun 2018 21:03
Last Modified:25 Sep 2018 16:16

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