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

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

doi:10.1038/s41396-018-0191-0

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

Journal Article · Wed Jun 13 00:00:00 EDT 2018 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-018-0191-0· OSTI ID:1468422

^[1]; Herrmann, Jonathan ^[2];

^[3]; Poitevin, Frédéric ^[4]; Ramdasi, Rasika ^[5]; Bargar, John R. ^[6]; Stahl, David A. ^[7]; Jensen, Grant J. ^[8]; Francis, Christopher A. ^[3]; Wakatsuki, Soichi ^[2];

^[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

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.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1468422

Journal Information:: The ISME Journal, Vol. 12, Issue 10; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 30 works

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