Conformational changes in a hyperthermostable glycoside hydrolase: enzymatic activity is a consequence of the loop dynamics and protonation balance

PLoS One. 2015 Feb 27;10(2):e0118225. doi: 10.1371/journal.pone.0118225. eCollection 2015.

Abstract

Endo-β-1, 4-mannanase from Thermotoga petrophila (TpMan) is a modular hyperthermostable enzyme involved in the degradation of mannan-containing polysaccharides. The degradation of these polysaccharides represents a key step for several industrial applications. Here, as part of a continuing investigation of TpMan, the region corresponding to the GH5 domain (TpManGH5) was characterized as a function of pH and temperature. The results indicated that the enzymatic activity of the TpManGH5 is pH-dependent, with its optimum activity occurring at pH 6. At pH 8, the studies demonstrated that TpManGH5 is a molecule with a nearly spherical tightly packed core displaying negligible flexibility in solution, and with size and shape very similar to crystal structure. However, TpManGH5 experiences an increase in radius of gyration in acidic conditions suggesting expansion of the molecule. Furthermore, at acidic pH values, TpManGH5 showed a less globular shape, probably due to a loop region slightly more expanded and flexible in solution (residues Y88 to A105). In addition, molecular dynamics simulations indicated that conformational changes caused by pH variation did not change the core of the TpManGH5, which means that only the above mentioned loop region presents high degree of fluctuations. The results also suggested that conformational changes of the loop region may facilitate polysaccharide and enzyme interaction. Finally, at pH 6 the results indicated that TpManGH5 is slightly more flexible at 65°C when compared to the same enzyme at 20°C. The biophysical characterization presented here is well correlated with the enzymatic activity and provide new insight into the structural basis for the temperature and pH-dependent activity of the TpManGH5. Also, the data suggest a loop region that provides a starting point for a rational design of biotechnological desired features.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Enzyme Activation
  • Enzyme Stability
  • Glycosides / metabolism
  • Hydrogen-Ion Concentration
  • Hydrolases / chemistry*
  • Hydrolases / metabolism
  • Models, Molecular*
  • Protein Conformation*
  • Structure-Activity Relationship
  • Temperature
  • Thermodynamics*

Substances

  • Glycosides
  • Hydrolases

Grants and funding

The authors would like to thank Fundação de Amparo a pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support for this work via grants #2011/13242-7, #2012/21054-9, #478900/2012-0, #2008/58037-9 and #2011/13242-7; and fellowships #2012/03503-0 (VMS) and #501037/2012-8 (FC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.