Elsevier

Journal of Theoretical Biology

Volume 244, Issue 1, 7 January 2007, Pages 127-132
Journal of Theoretical Biology

Adaptation of proteins to different environments: A comparison of proteome structural properties in Bacillus subtilis and Escherichia coli

https://doi.org/10.1016/j.jtbi.2006.07.021 Get rights and content

Abstract

We compared amino acid solvent accessibilities and helix propensities in data sets of Escherichia coli and Bacillus subtilis proteins. These species reside in very different environments and hold very different physiological properties. From the observations, it was proposed that the cytoplasm of B. subtilis is more ion-rich compared to the cytoplasm of E. coli, which might be more hydrophobic; therefore, during evolution these differences have resulted in different protein folding tracks. Such inherent differences imply that the results of bioinformatic analyses of protein structures might depend on the species from which the proteins are picked. It is also suggested that different cytoplasmic environments cause E. coli and B. subtilis to be appropriate for expression of distinct types of proteins.

Introduction

It is well-known that environmental conditions (e.g. temperature, pH, ionic strength, etc.) can affect peptide and protein structures in vitro. The effect of environmental conditions has been compensated for by evolution of sequences and structures that are best fitted to the living condition. For example, the frequency of certain amino acids can be significantly different in thermophilic and mesophilic organisms (Singer and Hickey, 2003), although a general pattern is not yet suggested (Vieille and Zeikus, 2001).

Each cell (or cellular compartment) can be considered as an “island” of biological macromolecules, enclosed by a membrane, which separates it from the surrounding environment. The environmental conditions inside the cells are dependent on cell types and specifically membrane proteins; hence, it is not odd to observe different evolutionary conditions applied on proteomes in different cell types. While the effect of temperature on the evolution of proteins has been studied vigorously (Vieille and Zeikus, 2001; Facchiano et al., 1998), to the best of our knowledge the effect of other environmental conditions has little been considered so far.

Here, we compared protein structure properties in two different microorganisms: Bacillus subtilis and Escherichia coli. They are both prokaryotes and lack internal compartments (e.g. nucleus, lysosome, etc.); this property makes them suitable for our study, since the internal organelles might hold different internal environments. Moreover, optimal growth temperatures of B. subtilis and E. coli are close (38.5 °C vs. 37 °C, respectively). Furthermore, B. subtilis is Gram-positive, while E. coli is Gram-negative, and their phylogenetic distance is substantial; hence, it is reasonable to expect differences between their cytoplasmic environments. For both organisms, there are enough resolved protein structures available to enable us to perform statistical analyses.

Section snippets

Non-redundant protein data sets

Eighty-four protein structures determined with resolutions of <2.5 Å and with sequence identity <30%, were chosen by searching for B. subtilis in the SOURCE section of PDB entries, followed by a culling procedure using PISCES server (Wang and Dunbrack, 2003; available from: http://www.fccc.edu/research/labs/dunbrack/pisces ). The method was repeated for E. coli, resulting in 456 proteins.

Extraction of amino acid properties

Secondary structures and accessible surface areas (ASA) of individual amino acids in selected proteins were

Amino acid ASAs are generally greater in B. subtilis, suggesting the existence of a more stabilizing cytoplasm in this organism

During evolution, proteins might become more flexible in a stabilizing environment compared to the proteins in destabilizing condition, which are selected to resist such condition; the latter proteins are expected to be more compact with a higher packing in their core (Li et al., 1998). As a result of their flexibility/rigidity states, their average magnitudes of amino acid solvent accessibilities are expected to be different (see Knapp et al., 1999): in an in vitro structure determination

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    Present address: New Ideas Research Institute, 11 Proshat Ave., Motahari St., Tehran, Iran.

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