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Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes.

ABSTRACT: Genomic correlates of evolutionary adaptation to very low or very high optimal growth temperature (OGT) values have been the subject of many studies. Whereas these provided a protein-structural rationale of the activity and stability of globular proteins/enzymes, the point has been neglected that adaptation to extreme temperatures could also have resulted from an increased use of intrinsically disordered proteins (IDPs), which are resistant to these conditions in vitro. Contrary to these expectations, we found a conspicuously low level of structural disorder in bacteria of very high (and very low) OGT values. This paucity of disorder does not reflect phylogenetic relatedness, i.e. it is a result of genuine adaptation to extreme conditions. Because intrinsic disorder correlates with important regulatory functions, we asked how these bacteria could exist without IDPs by studying transcription factors, known to harbor a lot of function-related intrinsic disorder. Hyperthermophiles have much less transcription factors, which have reduced disorder compared to their mesophilic counterparts. On the other hand, we found by systematic categorization of proteins with long disordered regions that there are certain functions, such as translation and ribosome biogenesis that depend on structural disorder even in hyperthermophiles. In all, our observations suggest that adaptation to extreme conditions is achieved by a significant functional simplification, apparent at both the level of the genome and individual genes/proteins.

SUBMITTER: Burra PV

PROVIDER: S-EPMC2920320 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes.

Burra Prasad V PV Kalmar Lajos L Tompa Peter P

PloS one 20100811 8

Genomic correlates of evolutionary adaptation to very low or very high optimal growth temperature (OGT) values have been the subject of many studies. Whereas these provided a protein-structural rationale of the activity and stability of globular proteins/enzymes, the point has been neglected that adaptation to extreme temperatures could also have resulted from an increased use of intrinsically disordered proteins (IDPs), which are resistant to these conditions in vitro. Contrary to these expecta ...[more]

PMID: 20711457

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Project description:The importance of unstructured biology has quickly grown during the last decades accompanying the explosion of the number of experimentally resolved protein structures. The idea that structural disorder might be a novel mechanism of protein interaction is widespread in the literature, although the number of statistically significant structural studies supporting this idea is surprisingly low. At variance with previous works, our conclusions rely exclusively on a large-scale analysis of all the 134337 X-ray crystallographic structures of the Protein Data Bank averaged over clusters of almost identical protein sequences. In this work, we explore the complexity of the organisation of all the interaction interfaces observed when a protein lies in alternative complexes, showing that interfaces progressively add up in a hierarchical way, which is reflected in a logarithmic law for the size of the union of the interface regions on the number of distinct interfaces. We further investigate the connection of this complexity with different measures of structural disorder: the standard missing residues and a new definition, called "soft disorder", that covers all the flexible and structurally amorphous residues of a protein. We show evidences that both the interaction interfaces and the soft disordered regions tend to involve roughly the same amino-acids of the protein, and preliminary results suggesting that soft disorder spots those surface regions where new interfaces are progressively accommodated by complex formation. In fact, our results suggest that structurally disordered regions not only carry crucial information about the location of alternative interfaces within complexes, but also about the order of the assembly. We verify these hypotheses in several examples, such as the DNA binding domains of P53 and P73, the C3 exoenzyme, and two known biological orders of assembly. We finally compare our measures of structural disorder with several disorder bioinformatics predictors, showing that these latter are optimised to predict the residues that are missing in all the alternative structures of a protein and they are not able to catch the progressive evolution of the disordered regions upon complex formation. Yet, the predicted residues, when not missing, tend to be characterised as soft disordered regions.

Project description:Vertebrate ectotherms such as reptiles provide ideal organisms for the study of adaptation to environmental thermal change. Comparative genomic and exomic studies can recover markers that diverge between warm and cold adapted lineages, but the genes that are functionally related to thermal adaptation may be difficult to identify. We here used a bioinformatics genome-mining approach to predict and identify functions for suitable candidate markers for thermal adaptation in the chicken. We first established a framework of candidate functions for such markers, and then compiled the literature on genes known to adapt to the thermal environment in different lineages of vertebrates. We then identified them in the genomes of human, chicken, and the lizard Anolis carolinensis, and established a functional genetic interaction network in the chicken. Surprisingly, markers initially identified from diverse lineages of vertebrates such as human and fish were all in close functional relationship with each other and more associated than expected by chance. This indicates that the general genetic functional network for thermoregulation and/or thermal adaptation to the environment might be regulated via similar evolutionarily conserved pathways in different vertebrate lineages. We were able to identify seven functions that were statistically overrepresented in this network, corresponding to four of our originally predicted functions plus three unpredicted functions. We describe this network as multimodal: central regulator genes with the function of relaying thermal signal (1), affect genes with different cellular functions, namely (2) lipoprotein metabolism, (3) membrane channels, (4) stress response, (5) response to oxidative stress, (6) muscle contraction and relaxation, and (7) vasodilation, vasoconstriction and regulation of blood pressure. This network constitutes a novel resource for the study of thermal adaptation in the closely related nonavian reptiles and other vertebrate ectotherms.

Dataset Information

Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes.

Publications

Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes.

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