Date Published: February 13, 2018
Publisher: Public Library of Science
Author(s): Dominik Schwarz, Orit Adato, Amnon Horovitz, Ron Unger, Chih-Horng Kuo.
The GroE chaperonin system, which comprises GroEL and GroES, assists protein folding in vivo and in vitro. It is conserved in all prokaryotes except in most, but not all, members of the class of mollicutes. In Escherichia coli, about 60 proteins were found to be obligatory clients of the GroE system. Here, we describe the properties of the homologs of these GroE clients in mollicutes and the evolution of chaperonins in this class of bacteria. Comparing the properties of these homologs in mollicutes with and without chaperonins enabled us to search for features correlated with the presence of GroE. Interestingly, no sequence-based features of proteins such as average length, amino acid composition and predicted folding/disorder propensity were found to be affected by the absence of GroE. Other properties such as genome size and number of proteins were also found to not differ between mollicute species with and without GroE. Our data suggest that two clades of mollicutes re-acquired the GroE system, thereby supporting the view that gaining the system occurred polyphyletically and not monophyletically, as previously debated. Our data also suggest that there might have been three isolated cases of lateral gene transfer from specific bacterial sources. Taken together, our data indicate that loss of GroE does not involve crossing a high evolutionary barrier and can be compensated for by a small number of changes within the few dozen client proteins.
Proteins can fold into their three-dimensional native structures spontaneously and without any assistance by other factors . In vivo, however, protein aggregation and mis-folding can occur owing to macromolecular crowding and other conditions that exist in cells. Protein mis-folding is harmful to cells because of the costs involved in the synthesis and degradation of non-functional proteins, toxic effects of protein aggregates (such as disruption of cell membranes ) and the absence of functional protein molecules that may have crucial roles. Hence, it is not surprising that selection against mis-folding is a major driving force in evolution . Molecular chaperones, which prevent aggregation and promote efficient protein folding, have, therefore, evolved and are found in all living cells [4,5]. The chaperone machineries that are involved in promoting protein substrate folding include the Hsp70 and Hsp90 systems and the chaperonins (Hsp60). These chaperones recognize regions that are exposed in non-native states of substrate proteins and they promote their folding by undergoing ATP-controlled cycles of protein substrate binding and release .
Many different comparisons can be made between E. coli clients and non-clients and their homologs in GroE+ and GroE- mollicute species (Fig 1). For example, E. coli clients can be compared with their homologs in GroE- mollicute species in order to uncover changes that occurred to compensate for the absence of GroE. Given, however, that E. coli and mollicutes are evolutionary distant and, thus, differ in many respects (e.g. GC content, codon usage, genome size etc.), a more controlled comparison is between the GroE+ and GroE- mollicute homologs. Thus, most of the analysis here was done in this manner but, for completeness, we also compared other groups in Fig 1 with regard to some properties.
Our analysis shows that 13 species of mollicutes are GroE+ and 46 are GroE-. Previous experimental studies [26,27] reported the existence of a GroEL homolog in Mycoplasma fermentans and Mycoplasma suis but we did not detect one in these species and, thus, classified them as GroE- (the existence of the GroE system in Mycoplasma suis has also been challenged before .