Origins of Life and Evolution of Biospheres

, Volume 44, Issue 4, pp 319–324 | Cite as

Molecular Crowding and Early Evolution

SPECIAL ISSUE OQOL 2014

Abstract

The environment of protocells might have been crowded with small molecules and functional and non-specific polymers. In addition to altering conformational equilibria, affecting reaction rates and changing the structure and activity of water, crowding might have enhanced the capabilities of protocells for evolutionary innovation through the creation of extended neutral networks in the fitness landscape.

Keywords

Crowding Excluded volume effect Protocell Vesicle Evolution Fitness landscape RNA Neutral network Evolutionary optimization 

Notes

Acknowledgments

This work was supported by the NASA Astrobiology Institute, the Simons Foundation (grant no. 290356 to IAC), the Foundational Questions in Evolutionary Biology Fund (grant no. RFP-12-05), the Searle Scholars Program, and the Institute for Collaborative Biotechnologies through grant W911NF-09-0001 from the U.S. Army Research Office. The content of the information does not necessarily reflect the position or the policy of the Government, and no official endorsement should be inferred.

References

  1. Adamala K, Szostak JW (2013) Nonenzymatic template-directed RNA synthesis inside model protocells. Science 342:1098–1100CrossRefPubMedCentralPubMedGoogle Scholar
  2. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5:593–599CrossRefPubMedCentralPubMedGoogle Scholar
  3. Chen IA, Salehi-Ashtiani K, Szostak JW (2005) RNA catalysis in model protocell vesicles. J Am Chem Soc 127:13213–13219CrossRefPubMedGoogle Scholar
  4. Cheung MS, Klimov D, Thirumalai D (2005) Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc Natl Acad Sci U S A 102:4753–4758CrossRefPubMedCentralPubMedGoogle Scholar
  5. Desai R, Kilburn D, Lee H-T, Woodson SA (2014) Increased ribozyme activity in crowded solutions. J Biol Chem 289(5):2972–2977CrossRefPubMedCentralPubMedGoogle Scholar
  6. Donahue CP, Yadava RS, Nesbitt SM, Fedor MJ (2000) The kinetic mechanism of the hairpin ribozyme in vivo: Influence of RNA helix stability on intracellular cleavage kinetics. J Mol Biol 295:693–707CrossRefPubMedGoogle Scholar
  7. Ellington AD, Chen X, Robertson M, Syrett A (2009) Evolutionary origins and directed evolution of RNA. Int J Biochem Cell Biol 41:254–265CrossRefPubMedGoogle Scholar
  8. Ellis RJ (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11:114–119CrossRefPubMedGoogle Scholar
  9. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton Univ Press, PrincetonGoogle Scholar
  10. Jiménez JI, Xulvi-Brunet R, Campbell GW, Turk-MacLeod R, Chen IA (2013) Comprehensive experimental fitness landscape and evolutionary network for small RNA. Proc Natl Acad Sci U S A 110:14984–14989CrossRefPubMedCentralPubMedGoogle Scholar
  11. Kilburn D, Roh JH, Behrouzi R, Briber RM, Woodson SA (2013) Crowders perturb the entropy of RNA energy landscapes to favor folding. J Am Chem Soc 135:10055–10063CrossRefPubMedCentralPubMedGoogle Scholar
  12. Lareu RR, Harve KS, Raghunath M (2007) Emulating a crowded intracellular environment in vitro dramatically improves RT-PCR performance. Biochem Biophys Res Commun 363:171–177CrossRefPubMedGoogle Scholar
  13. Maynard Smith J (1970) Natural selection and the concept of a protein space. Nature 225:563–564CrossRefGoogle Scholar
  14. Minton AP (1981) Excluded volume as a determinant of macromolecular structure and reactivity. Biopolymers 20:2093–2120CrossRefGoogle Scholar
  15. Minton AP (1998) [7] Molecular crowding: Analysis of effects of high concentrations of inert cosolutes on biochemical equilibria and rates in terms of volume exclusion. In: Gary K. Ackers MLJ (ed) Methods Enzymol., vol 295. Academic Press, pp 127–149Google Scholar
  16. Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biological reactions in physiological media. J Biol Chem 276:10577–10580CrossRefPubMedGoogle Scholar
  17. Munishkina LA, Cooper EM, Uversky VN, Fink AL (2004) The effect of macromolecular crowding on protein aggregation and amyloid fibril formation. J Mol Recognit 17:456–464CrossRefPubMedGoogle Scholar
  18. Muramatsu N, Minton AP (1988) Tracer diffusion of globular proteins in concentrated protein solutions. Proc Natl Acad Sci U S A 85:2984–2988CrossRefPubMedCentralPubMedGoogle Scholar
  19. Nakano S-i, Karimata HT, Kitagawa Y, Sugimoto N (2009) Facilitation of RNA enzyme activity in the molecular crowding media of cosolutes. J Am Chem Soc 131:16881–16888CrossRefPubMedGoogle Scholar
  20. Nakano S-i, Miyoshi D, Sugimoto N (2013) Effects of molecular crowding on the structures, interactions, and functions of nucleic acids. Chem Rev 114:2733–2758CrossRefPubMedGoogle Scholar
  21. Pohorille A, Pratt LR (2012) Is water the universal solvent for life? Orig Life Evol Biosph 42:405–409CrossRefPubMedGoogle Scholar
  22. Rendel MD (2011) Adaptive evolutionary walks require neutral intermediates in RNA fitness landscapes. Theor Popul Biol 79:12–18CrossRefPubMedGoogle Scholar
  23. Saha R, Rakshit S, Verma PK, Mitra RK, Pal SK (2013) Protein-cofactor binding and ultrafast electron transfer in riboflavin binding protein under the spatial confinement of nanoscopic reverse micelles. J Mol Recognit 26:59–66CrossRefPubMedGoogle Scholar
  24. Saha R, Verma PK, Mitra RK, Pal SK (2011) Structural and dynamical characterization of unilamellar AOT vesicles in aqueous solutions and their efficacy as potential drug delivery vehicle. Colloids Surf B 88:345–353CrossRefGoogle Scholar
  25. Sarkar M, Li C, Pielak G (2013) Soft interactions and crowding. Biophys Rev 5:187–194CrossRefGoogle Scholar
  26. Schuster P (2011) Mathematical modeling of evolution. Solved and open problems. Theory Biosci 130:71–89CrossRefPubMedGoogle Scholar
  27. Schuster P, Fontana W, Stadler PF, Hofacker IL (1994) From sequences to shapes and back: A case study in RNA secondary structures. Proc R Soc Lond B 255:279–284CrossRefGoogle Scholar
  28. Senske M, Törk L, Born B, Havenith M, Herrmann C, Ebbinghaus S (2014) Protein stabilization by macromolecular crowding through enthalpy rather than entropy. J Am Chem Soc 136:9036–9041CrossRefPubMedGoogle Scholar
  29. Strulson CA, Molden RC, Keating CD, Bevilacqua PC (2012) RNA catalysis through compartmentalization. Nat Chem 4:941–946CrossRefPubMedGoogle Scholar
  30. Strulson CA, Yennawar NH, Rambo RP, Bevilacqua PC (2013) Molecular crowding favors reactivity of a human ribozyme under physiological ionic conditions. Biochemistry 52:8187–8197CrossRefPubMedGoogle Scholar
  31. Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409:387–390CrossRefPubMedGoogle Scholar
  32. Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99PubMedCentralPubMedGoogle Scholar
  33. Tyrrell J, McGinnis JL, Weeks KM, Pielak GJ (2013) The cellular environment stabilizes adenine riboswitch RNA structure. Biochemistry 52:8777–8785CrossRefPubMedGoogle Scholar
  34. Verma PK, Saha R, Mitra RK, Pal SK (2010) Slow water dynamics at the surface of macromolecular assemblies of different morphologies. Soft Matter 6:5971–5979CrossRefGoogle Scholar
  35. Wang Y, Sarkar M, Smith AE, Krois AS, Pielak GJ (2012) Macromolecular crowding and protein stability. J Am Chem Soc 134:16614–16618CrossRefPubMedGoogle Scholar
  36. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedCentralPubMedGoogle Scholar
  37. Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222:599–620CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Ranajay Saha
    • 1
  • Andrew Pohorille
    • 2
  • Irene A. Chen
    • 1
    • 3
  1. 1.Department of Chemistry and BiochemistryUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Exobiology BranchNASA Ames Research CenterMoffett FieldUSA
  3. 3.Program in Biomolecular Sciences and EngineeringUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations