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Title: 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 » broad implications for comparisons of ecologically distinct populations.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3];  [4];  [5];  [6];  [7];  [8];  [3];  [2]; ORCiD logo [9]
  1. Stanford Univ., Stanford, CA (United States). Dept. of Electrical Engineering; SLAC National Accelerator Lab., Menlo Park, CA (United States)
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States); Stanford Univ., Stanford, CA (United States). Dept. of Structural Biology
  3. Stanford Univ., Stanford, CA (United States). Dept. of Earth System Science
  4. Stanford Univ., Stanford, CA (United States). Dept. of Structural Biology; SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford PULSE Inst.
  5. California Inst. of Technology, Pasadena, CA (United States). Division of Biology and Biological Engineering
  6. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  7. Univ. of Washington, Seattle, WA (United States). Dept. of Civil and Environmental Engineering
  8. 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.
  9. 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}
}

Journal Article:
Free Publicly Available Full Text
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Citation Metrics:
Cited by: 4 works
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Figures / Tables:

Fig. 1 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 » or positive charge at neutral pH. c Zeta potential measurements of living N. limnia SFB1 cells in growth medium plotted as a function of pH. The absolute value of the potential is reported. Error bars show the length of one standard deviation« less

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    Works referencing / citing this record:

    CRISPR-mediated gene silencing reveals involvement of the archaeal S-layer in cell division and virus infection
    journal, October 2019


    A bacterial surface layer protein exploits multistep crystallization for rapid self-assembly
    journal, December 2019


    Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical sponge Ianthella basta
    journal, July 2019


    Candidatus Nitrosotenuis aquarius,” an Ammonia-Oxidizing Archaeon from a Freshwater Aquarium Biofilter
    journal, June 2018


    Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly
    journal, June 2019


    Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier
    journal, February 2020


    Affinity informs environmental cooperation between ammonia-oxidizing archaea (AOA) and anaerobic ammonia-oxidizing (Anammox) bacteria
    journal, April 2019


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.