Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins
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, withmore »
- Authors:
-
[1];
[3];
[9]
- Stanford Univ., Stanford, CA (United States). Dept. of Electrical Engineering; SLAC National Accelerator Lab., Menlo Park, CA (United States)
- SLAC National Accelerator Lab., Menlo Park, CA (United States); Stanford Univ., Stanford, CA (United States). Dept. of Structural Biology
- Stanford Univ., Stanford, CA (United States). Dept. of Earth System Science
- Stanford Univ., Stanford, CA (United States). Dept. of Structural Biology; SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford PULSE Inst.
- California Inst. of Technology, Pasadena, CA (United States). Division of Biology and Biological Engineering
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Univ. of Washington, Seattle, WA (United States). Dept. of Civil and Environmental Engineering
- California Inst. of Technology, Pasadena, CA (United States). Division of Biology and Biological Engineering; California Inst. of Technology, Pasadena, CA (United States). Howard Hughes Medical Inst.
- SLAC National Accelerator Lab., Menlo Park, CA (United States); Univ. of California, San Francisco, CA (United States). Dept. of Bioengineering and Therapeutic Sciences
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1468422
- Grant/Contract Number:
- AC02-76SF00515
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 10; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Li, Po-Nan, Herrmann, Jonathan, Tolar, Bradley B., Poitevin, Frédéric, Ramdasi, Rasika, Bargar, John R., Stahl, David A., Jensen, Grant J., Francis, Christopher A., Wakatsuki, Soichi, and van den Bedem, Henry. Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins. United States: N. p., 2018.
Web. doi:10.1038/s41396-018-0191-0.
Li, Po-Nan, Herrmann, Jonathan, Tolar, Bradley B., Poitevin, Frédéric, Ramdasi, Rasika, Bargar, John R., Stahl, David A., Jensen, Grant J., Francis, Christopher A., Wakatsuki, Soichi, & van den Bedem, Henry. Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins. United States. https://doi.org/10.1038/s41396-018-0191-0
Li, Po-Nan, Herrmann, Jonathan, Tolar, Bradley B., Poitevin, Frédéric, Ramdasi, Rasika, Bargar, John R., Stahl, David A., Jensen, Grant J., Francis, Christopher A., Wakatsuki, Soichi, and van den Bedem, Henry. Wed .
"Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins". United States. https://doi.org/10.1038/s41396-018-0191-0. https://www.osti.gov/servlets/purl/1468422.
@article{osti_1468422,
title = {Nutrient transport suggests an evolutionary basis for charged archaeal surface layer proteins},
author = {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},
abstractNote = {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 (NH4+), we find that the characteristic length scales of nanoporous S-layers elevate the concentration of NH4+ 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 NH4+ availability, with broad implications for comparisons of ecologically distinct populations.},
doi = {10.1038/s41396-018-0191-0},
url = {https://www.osti.gov/biblio/1468422},
journal = {The ISME Journal},
issn = {1751-7362},
number = 10,
volume = 12,
place = {United States},
year = {2018},
month = {6}
}
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Figures / Tables:
Fig. 1: SLPs share a propensity for charged amino acids, despite exceptional sequence diversity. a Amino-acid sequence identity matrix for putative S-layer proteins from all known archaeal clades. Color codes indicate the % identity. b Isoelectric points for the SLPs analyzed in a show clusters of sequences with notable negativemore »
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