A Comparison of Structural and Evolutionary Attributes of Escherichia coli and Thermus thermophilus Small Ribosomal Subunits: Signatures of Thermal Adaptation

Abstract

Here we compare the structural and evolutionary attributes of Thermus thermophilus and Escherichia coli small ribosomal subunits (SSU). Our results indicate that with few exceptions, thermophilic 16S ribosomal RNA (16S rRNA) is densely packed compared to that of mesophilic at most of the analogous spatial regions. In addition, we have located species-specific cavity clusters (SSCCs) in both species. E. coli SSCCs are numerous and larger compared to T. thermophilus SSCCs, which again indicates densely packed thermophilic 16S rRNA. Thermophilic ribosomal proteins (r-proteins) have longer disordered regions than their mesophilic homologs and they experience larger disorder-to-order transitions during SSU-assembly. This is reflected in the predicted higher conformational changes of thermophilic r-proteins compared to their mesophilic homologs during SSU-assembly. This high conformational change of thermophilic r-proteins may help them to associate with the 16S ribosomal RNA with high complementary interfaces, larger interface areas, and denser molecular contacts, compared to those of mesophilic. Thus, thermophilic protein-rRNA interfaces are tightly associated with 16S rRNA than their mesophilic homologs. Densely packed 16S rRNA interior and tight protein-rRNA binding of T. thermophilus (compared to those of E. coli) are likely the signatures of its thermal adaptation. We have found a linear correlation between the free energy of protein-RNA interface formation, interface size, and square of conformational changes, which is followed in both prokaryotic and eukaryotic SSU. Disorder is associated with high protein-RNA interface polarity. We have found an evolutionary tendency to maintain high polarity (thereby disorder) at protein-rRNA interfaces, than that at rest of the protein structures. However, some proteins exhibit exceptions to this general trend.

Structural Basis of the Subcellular Topology Landscape of Escherichia coli

“…Additionally, enhanced inherent disorder and flexibility may satisfy a third purpose of specific cell envelope related functions (Supplementary Table S9), e.g., binding prosthetic groups (e.g., NrfB; Clarke et al, 2007), chaperoning (Skp, Spy, SurA, PpiA, HdeA; Walton and Sousa, 2004; Burmann et al, 2013), interaction with OM proteins and conformational linkage to the IM (TonB; Sean Peacock et al, 2005), sensing stress (RcsF; Rogov et al, 2011), peptidoglycan binding and periplasm-cell surface topological transitions (Lpp; Liu et al, 2002); small molecule (Tompa et al, 2006) and colicin (Johnson et al, 2017) import and phage adsorption (DcrB; Likhacheva et al, 1996), lateral Bam opening to facilitate porin insertion (Hagan et al, 2011), curli subunits that are additionally secreted across the OM like the amyloid fiber CsgA and the CsgF lid (Raivio et al, 1999; Van Gerven et al, 2015). Disorder can also have additional relevant functions, e.g., by facilitating multiple interactions it can yield higher thermostability as in the small ribosomal subunits of Thermus thermophilus when compared to those of the mesophilic E. coli (Mallik and Kundu, 2013).…”

Evolution of Protein Structure and Stability in Global Warming

“…Although folding and refolding can be achieved with purified proteins in vitro, the role of the intracellular environment and interacting proteins, such as chaperons [ 23 , 24 ], which are relevant for a real-life survival, cannot be ignored. Many proteins also interact with RNA, both large and small, and a large variety of small molecules can act as regulators and modifiers [ 25 , 26 ]. Given these caveats, we should at least focus on studies comparing orthologous proteins in closely related species.…”

Structural signatures of thermal adaptation of bacterial ribosomal RNA, transfer RNA, and messenger RNA

“…Dutta and Chaudhuri showed that the secondary structure of tRNA was more stably folded [ 33 ]. Mallik and Kundu found that the tertiary structure of thermophilic 16S rRNA is more packed than that of mesophilic one [ 34 ]. Limited knowledge is largely due to the fact that RNA structures are challenging to determine experimentally while computational prediction of tertiary structure is far from accurate [ 35 ].…”

“…This is a generally accepted practice as there is simple no other alternative to analyze temperature-dependent behavior. For example, thermophilic and mesophilic 16S rRNAs were compared directly, despite that they were crystalized at the same temperature of 277K [ 34 ]. Here, we showed that rRNA and tRNA have very different temperature adaptation from mRNA.…”