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 (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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References

  1. 1.

    Sleytr UB, Sára M. Bacterial and archaeal s-layer proteins: structure-function relationships and their biotechnological applications. Trends Biotechnol. 1997;15:20–6.

  2. 2.

    Albers SV, Meyer BH. The archaeal cell envelope. Nat Rev Microbiol. 2011;9:414–26.

  3. 3.

    Madhurantakam C, Howorka S, Remaut H. S-layer structure in bacteria and archaea. In: Barton L., Bazylinski D., Xu H. (eds) Nanomicrobiology. Springer, NY, New York, 2014. p. 11–37.

  4. 4.

    Fagan RP, Fairweather NF. Biogenesis and functions of bacterial S-layers. Nat Rev Microbiol. 2014;12:211–22.

  5. 5.

    McDougall M, Francisco O, Viddal C, Roshko R, Meier M, Stetefeld J. Archaea S-layer nanotube from a “black smoker” in complex with cyclo-octasulfur S8 rings. Proteins. 2017;85:2209–16.

  6. 6.

    Gerbino E, Carasi P, Mobili P, Serradell MA, Gómez-Zavaglia A. Role of S-layer proteins in bacteria. World J Microbiol Biotechnol. 2015;31:1877–87.

  7. 7.

    König H. Archaeobacterial cell envelopes. Can J Microbiol. 1988;34:395–406.

  8. 8.

    Engelhardt H. Mechanism of osmoprotection by archaeal s-layers: a theoretical study. J Struct Biol. 2007;160:190–9.

  9. 9.

    Kish A, Miot J, Lombard C, Guigner JM, Bernard S, Zirah S, et al. Preservation of archaeal surface layer structure during mineralization. Sci Rep. 2016;6:26152.

  10. 10.

    Sára M, Sleytr UB. Molecular sieving through S-layers of bacillus stearothermophilus strains. J Bacteriol. 1987;169:4092–8.

  11. 11.

    Nikaido H, Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol Rev. 1985;49:1–32.

  12. 12.

    Sotiropoulou S, Mark SS, Angert ER, Batt CA. Nanoporous S-layer protein lattices. A biological ion gate with calcium selectivity. J Phys Chem C. 2007;111:13232–7.

  13. 13.

    Tagliazucchi M, Szleifer I. Transport mechanisms in nanopores and nanochannels: can we mimic nature? Mater Today. 2015;18:131–42.

  14. 14.

    Valentine DL. Adaptations to energy stress dictate the ecology and evolution of the archaea. Nat Rev Microbiol. 2007;5:316–23.

  15. 15.

    Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the thaumarchaeota. Nat Rev Microbiol. 2008;6:245–52.

  16. 16.

    Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 2006;442:806–9.

  17. 17.

    Wuchter C, Abbas B, Coolen MJL, Herfort L, Bleijswijk J, van Timmers P, et al. Archaeal nitrification in the ocean. Proc Natl Acad Sci USA. 2006;103:12317–22.

  18. 18.

    Michael Beman J, Popp BN, Francis CA. Molecular and biogeochemical evidence for ammonia oxidation by marine crenarchaeota in the gulf of california. ISME J. 2008;2:429–41.

  19. 19.

    Stahl DA, Torre JRdela. Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol. 2012;66:83–101.

  20. 20.

    Prosser JI, Nicol GW. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol. 2008;10:2931–41.

  21. 21.

    Santoro AE, Casciotti KL, Francis CA. Activity, abundance and diversity of nitrifying archaea and bacteria in the central california current. Environ Microbiol. 2010;12:1989–2006.

  22. 22.

    Martens-Habbena W, Berube PM, Urakawa H, Torre JRdela, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature. 2009;461:976–9.

  23. 23.

    Horak REA, Qin W, Schauer AJ, Armbrust EV, Ingalls AE, Moffett JW, et al. Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by archaea. ISME J. 2013;7:2023–33.

  24. 24.

    Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damste JS, Rhee SK. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol. 2010;76:7575–87.

  25. 25.

    Sato C, Schnoor JL, McDonald DB, Huey J. Test medium for the growth of nitrosomonas europaea. Appl Environ Microbiol. 1985;49:1101–7.

  26. 26.

    Ward BB. Kinetic studies on ammonia and methane oxidation by Nitrosococcus oceanus. Arch Microbiol. 1987;147:126–33.

  27. 27.

    Sayavedra-Soto L, Arp D. Ammonia-oxidizing bacteria: their biochemistry and molecular biology. In: Ward B, Arp D, Klotz M, (eds). Nitrification. ASM Press, DC, Washington, 2011. p. 11–37.

  28. 28.

    Kerou M, Offre P, Valledor L, Abby SS, Melcher M, Nagler M, et al. Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers. Proc Natl Acad Sci USA. 2016;113:E7937–46.

  29. 29.

    Lehtovirta-Morley LE, Sayavedra-Soto LA, Gallois N, Schouten S, Stein LY, Prosser JI, et al. Identifying potential mechanisms enabling acidophily in the ammonia-oxidizing archaeon “Candidatus Nitrosotalea devanaterra”. Appl Environ Microbiol. 2016;82:2608–19.

  30. 30.

    Tolar BB, Herrmann J, Bargar JR, van den Bedem H, Wakatsuki S, Francis CA. Integrated structural biology and molecular ecology of N-cycling enzymes from ammonia-oxidizing archaea. Environ Microbiol Rep. 2017;9:484–91.

  31. 31.

    Walker CB, Torre JR, de la, Klotz MG, Urakawa H, Pinel N, Arp DJ, et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA. 2010;107:8818–23.

  32. 32.

    Suzuki I, Dular U, Kwok SC. Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J Bacteriol. 1974;120:556–8.

  33. 33.

    Hatzenpichler R. Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol. 2012;78:7501–10.

  34. 34.

    Gorman-Lewis D, Martens-Habbena W, Stahl DA. Thermodynamic characterization of proton-ionizable functional groups on the cell surfaces of ammonia-oxidizing bacteria and archaea. Geobiology. 2014;12:157–71.

  35. 35.

    Daiguji H, Yang P, Majumdar A. Ion transport in nanofluidic channels. Nano Lett. 2004;4:137–42.

  36. 36.

    Stein D, Kruithof M, Dekker C. Surface-charge-governed ion transport in nanofluidic channels. Phys Rev Lett. 2004;93:035901.

  37. 37.

    Ho C, Qiao R, Heng JB, Chatterjee A, Timp RJ, Aluru NR, et al. Electrolytic transport through a synthetic nanometer-diameter pore. Proc Natl Acad Sci USA. 2005;102:10445–50.

  38. 38.

    Duan C, Majumdar A. Anomalous ion transport in 2-nm hydrophilic nano channels. Nat Nanotechnol. 2010;5:848–52.

  39. 39.

    Mosier AC, Lund MB, Francis CA. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb Ecol. 2012;64:955–63.

  40. 40.

    Herrmann J, Jabbarpour F, Bargar PG, Nomellini JF, Li PN, Lane TJ, et al. Environmental calcium controls alternate physical states of the caulobacter surface layer. Biophys J. 2017;112:1841–51.

  41. 41.

    Calo D, Kaminski L, Eichler J. Protein glycosylation in archaea: sweet and extreme. Glycobiology. 2010;20:1065–76.

  42. 42.

    Peyfoon, E, Meyer, B, Hitchen, PG, Panico, M, Morris, HR, Haslam, SM, et al. The S-layer glycoprotein of the crenarchaeote Sulfolobus acidocaldarius is glycosylated at multiple sites with chitobiose-linked N-glycans. Archaea 2010.

  43. 43.

    Baumeister W, Wildhaber I, Phipps BM. Principles of organization in eubacterial and archaebacterial surface proteins. Can J Microbiol. 1989;35:215–27.

  44. 44.

    Qin W, Amin SA, Lundeen RA, Heal KR, Martens-Habbena W, Turkarslan S, et al. Stress response of a marine ammonia-oxidizing archaeon informs physiological status of environmental populations. ISME J. 2018;12:508–19.

  45. 45.

    Krogh A, Larsson B, Heijne Gvon, Sonnhammer EL. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol. 2001;305:567–80.

  46. 46.

    Yachdav G, Kloppmann E, Kajan L, Hecht M, Goldberg T, Hamp T, et al. PredictProtein-an open resource for online prediction of protein structural and functional features. Nucleic Acids Res. 2014;42:W337–43.

  47. 47.

    Eichler J, Maupin-Furlow J. Post-translation modification in archaea: lessons from haloferax volcanii and other haloarchaea. FEMS Microbiol Rev. 2013;37:583–606.

  48. 48.

    Arbing MA, Chan S, Shin A, Phan T, Ahn CJ, Rohlin L, et al. Structure of the surface layer of the methanogenic archaean methanosarcina acetivorans. Proc Natl Acad Sci USA. 2012;109:11812–7.

  49. 49.

    Bharat TAM, Kureisaite-Ciziene D, Hardy GG, Yu EW, Devant JM, Hagen WJH, et al. Structure of the hexagonal surface layer on caulobacter crescentus cells. Nat Microbiol. 2017;2:17059.

  50. 50.

    Galdiero S, Falanga A, Cantisani M, Tarallo R, Della Pepa ME, D'Oriano V, et al. Microbe-host interactions: structure and role of gram-negative bacterial porins. Curr Protein Pept Sci. 2012;13:843–54.

  51. 51.

    Benz R, Schmid A, Hancock RE. Ion selectivity of gram-negative bacterial porins. J Bacterid. 1985;162:722–7.

  52. 52.

    Ritchie RJ. The ammonia transport, retention and futile cycling problem in cyanobacteria. Microb Ecol. 2013;65:180–96.

  53. 53.

    Im W, Roux B. Ion permeation and selectivity of OmpF porin: a theoretical study based on molecular dynamics, brownian dynamics, and continuum electrodiffusion theory. J Mol Biol. 2002a;322:851–69.

  54. 54.

    Im W, Roux B. Ions and counterions in a biological channel: a molecular dynamics simulation of OmpF porin from Escherichia coli in an explicit membrane with 1 M KCl aqueous salt solution. J Mol Biol. 2002b;319:1177–97.

  55. 55.

    Bernhard AE, Landry ZC, Blevins A, Torre JR, de la, Giblin AE, Stahl DA. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol. 2010;76:1285–9.

  56. 56.

    Rysgaard S, Thastum P, Dalsgaard T, Christensen PB, Sloth NP. Effects of salinity on NH4+ adsorption capacity, nitrification, and denitrification in Danish estuarine sediments. Estuaries. 1999;22:21–30.

  57. 57.

    Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and thaumarchaeota. ISME J. 2016;10:1836–45.

  58. 58.

    Martens-Habbena W, Qin W, Horak REA, Urakawa H, Schauer AJ, Moffett JW, et al. The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger. Environ Microbiol. 2015;17:2261–74.

  59. 59.

    Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, et al. Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J. 2014;8:1135–46.

  60. 60.

    van den Bedem H, Fraser JS. Integrative, dynamic structural biology at atomic resolution— it's about time. Nat Methods. 2015;12:307–18.

  61. 61.

    Offre P, Kerou M, Spang A, Schleper C. Variability of the transporter gene complement in ammonia-oxidizing archaea. Trends Microbiol. 2014;22:665–75.

  62. 62.

    Iancu CV, Tivol WF, Schooler JB, Dias DP, Henderson GP, Murphy GE, et al. Electron cryotomography sample preparation using the vitrobot. Nat Protoc. 2006;1:2813–9.

  63. 63.

    Mastronarde, DN. Fiducial marker and hybrid alignment methods for single- and double-axis tomography. In: Frank J. (ed) Electron tomography. Springer, NY, New York, 2007. p. 163–85.

  64. 64.

    Nicastro D, Schwartz C, Pierson J, Gaudette R, Porter ME, McIntosh JR. The molecular architecture of axonemes revealed by cryoelectron tomography. Science. 2006;313:944–8.

  65. 65.

    Cohen H, Cooley JW. The numerical solution of the time-dependent Nernst-Planck equations. Biophys J. 1965;5:145–62.

  66. 66.

    Brumleve TR, Buck RP. Numerical solution of the Nernst-Planck and poisson equation system with applications to membrane electrochemistry and solid state physics. J Electroanal Chem Interfacial Electrochem. 1978;90:1–31.

  67. 67.

    Lu B, Holst MJ, McCammon JA, Zhou YC. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol. 2010;76:7575–87.

  68. 68.

    Lelidis I, Ross Macdonald J, Barbero G. Poisson–Nernst-Planck model with Chang-Jaffe, diffusion, and ohmic boundary conditions. J Phys D Appl Phys. 2015;49:025503.

  69. 69.

    Song J, Tan H, Mahmood K, Law RHP, Buckle AM, Webb GI, et al. Prodepth: predict residue depth by support vector regression approach from protein sequences only. PLoS One. 2009;4:e7072.

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Acknowledgements

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).

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Affiliations

  1. Department of Electrical Engineering, Stanford University, Stanford, CA, 94305, USA

    • Po-Nan Li
  2. SLAC National Accelerator Laboratory, Menlo Park, CA, 94025, USA

    • Po-Nan Li
    • , Jonathan Herrmann
    • , John R. Bargar
    • , Soichi Wakatsuki
    •  & Henry van den Bedem
  3. Department of Structural Biology, Stanford University, Stanford, CA, 94305, USA

    • Jonathan Herrmann
    • , Frédéric Poitevin
    •  & Soichi Wakatsuki
  4. Department of Earth System Science, Stanford University, Stanford, CA, 94305, USA

    • Bradley B. Tolar
    •  & Christopher A. Francis
  5. Stanford PULSE Institute, SLAC National Accelerator Laboratory, Menlo Park, CA, 94025, USA

    • Frédéric Poitevin
  6. Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, 91125, USA

    • Rasika Ramdasi
    •  & Grant J. Jensen
  7. Department of Civil and Environmental Engineering, University of Washington, Seattle, WA, 98195, USA

    • David A. Stahl
  8. Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA, 91125, USA

    • Grant J. Jensen
  9. Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, CA, 94158, USA

    • Henry van den Bedem

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The authors declare that they have no conflict of interest.

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Correspondence to Christopher A. Francis or Soichi Wakatsuki or Henry van den Bedem.

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https://doi.org/10.1038/s41396-018-0191-0