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Essential functions linked with structural disorder in organisms of minimal genome

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ABSTRACT

Abstract: Intrinsically disordered regions (IDRs) of proteins fulfill important regulatory roles in most organisms. However, the proteins of certain endosymbiont and intracellular pathogenic bacteria with extremely reduced genomes contain disproportionately small amounts of IDRs, consisting almost entirely of folded domains. As their genomes co-evolving with their hosts have been reduced in unrelated lineages, the proteomes of these bacteria represent independently evolved minimal protein sets. We systematically analyzed structural disorder in a representative set of such minimal organisms to see which types of functionally relevant longer IDRs are invariably retained in them. We found that a few characteristic functions are consistently linked with conformational disorder: ribosomal proteins, key components of the protein production machinery, a central coordinator of DNA metabolism and certain housekeeping chaperones seem to strictly rely on structural disorder even in genome-reduced organisms. We propose that these functions correspond to the most essential and probably also the most ancient ones fulfilled by structural disorder in cellular organisms.

Reviewers: This article was reviewed by Michael Gromiha, Zoltan Gaspari and Sandor Pongor.

Electronic supplementary material: The online version of this article (doi:10.1186/s13062-016-0149-y) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus

Conserved disorder in chaperones and hub proteins of minimal organisms. Domain maps, structures, sequence and disorder conservation are depicted for the three proteins (GroEL (a) DnaK (b) and SSB (c)) with conserved long disordered regions. On the grey domain maps, the residue boundaries of conserved disordered segments (in red) and known domains (in darker grey) are provided. The red regions of the domain maps complemented by a few residue positions around are also highlighted as Clustal Omega 1.2.2. multiple sequence alignments below the domain maps. The sequences of the minimal and reference organisms are identified by their Taxonomy/UniProt identifiers, and are depicted in the same order as in Table 1. In the alignments the background of the residues are colored according to the corresponding IUPred predictions; residues with a score >0.5 in darker red, while residues with a score between 0.5 and 0.4 in lighter red. The structures of the corresponding E. coli proteins (PDB: 2NWC for GroEL, 2KHO for DnaK and 1QVC for SSB) are also depicted in light grey with the conserved disordered segments marked by red or added as red dashed lines. In the heptameric GroEL and tetrameric SSB structures one chain is depicted by darker grey than the others
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Fig1: Conserved disorder in chaperones and hub proteins of minimal organisms. Domain maps, structures, sequence and disorder conservation are depicted for the three proteins (GroEL (a) DnaK (b) and SSB (c)) with conserved long disordered regions. On the grey domain maps, the residue boundaries of conserved disordered segments (in red) and known domains (in darker grey) are provided. The red regions of the domain maps complemented by a few residue positions around are also highlighted as Clustal Omega 1.2.2. multiple sequence alignments below the domain maps. The sequences of the minimal and reference organisms are identified by their Taxonomy/UniProt identifiers, and are depicted in the same order as in Table 1. In the alignments the background of the residues are colored according to the corresponding IUPred predictions; residues with a score >0.5 in darker red, while residues with a score between 0.5 and 0.4 in lighter red. The structures of the corresponding E. coli proteins (PDB: 2NWC for GroEL, 2KHO for DnaK and 1QVC for SSB) are also depicted in light grey with the conserved disordered segments marked by red or added as red dashed lines. In the heptameric GroEL and tetrameric SSB structures one chain is depicted by darker grey than the others

Mentions: Interestingly, chaperones seem to rely on structural disorder the most. For example, the C-terminal tail of GroEL preserved its disordered nature in most minimal and reference species (Fig. 1a). Although the E. coli sequence is not predicted as disordered, this is certainly a misprediction because the respective region is missing from available X-ray structures (Fig. 1a). The highly flexible, hydrophilic tails protrude into the cavity of the ball-shaped chaperonin cage formed by GroEL/GroES subunits and assist the correct folding of proteins [36]. Multiple studies collectively confirmed that truncation of the tail impairs the efficient refolding of substrate proteins [36–39], however its specific molecular role in the chaperonin reaction cycle is still under debate [38, 39].Fig. 1


Essential functions linked with structural disorder in organisms of minimal genome
Conserved disorder in chaperones and hub proteins of minimal organisms. Domain maps, structures, sequence and disorder conservation are depicted for the three proteins (GroEL (a) DnaK (b) and SSB (c)) with conserved long disordered regions. On the grey domain maps, the residue boundaries of conserved disordered segments (in red) and known domains (in darker grey) are provided. The red regions of the domain maps complemented by a few residue positions around are also highlighted as Clustal Omega 1.2.2. multiple sequence alignments below the domain maps. The sequences of the minimal and reference organisms are identified by their Taxonomy/UniProt identifiers, and are depicted in the same order as in Table 1. In the alignments the background of the residues are colored according to the corresponding IUPred predictions; residues with a score >0.5 in darker red, while residues with a score between 0.5 and 0.4 in lighter red. The structures of the corresponding E. coli proteins (PDB: 2NWC for GroEL, 2KHO for DnaK and 1QVC for SSB) are also depicted in light grey with the conserved disordered segments marked by red or added as red dashed lines. In the heptameric GroEL and tetrameric SSB structures one chain is depicted by darker grey than the others
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5016991&req=5

Fig1: Conserved disorder in chaperones and hub proteins of minimal organisms. Domain maps, structures, sequence and disorder conservation are depicted for the three proteins (GroEL (a) DnaK (b) and SSB (c)) with conserved long disordered regions. On the grey domain maps, the residue boundaries of conserved disordered segments (in red) and known domains (in darker grey) are provided. The red regions of the domain maps complemented by a few residue positions around are also highlighted as Clustal Omega 1.2.2. multiple sequence alignments below the domain maps. The sequences of the minimal and reference organisms are identified by their Taxonomy/UniProt identifiers, and are depicted in the same order as in Table 1. In the alignments the background of the residues are colored according to the corresponding IUPred predictions; residues with a score >0.5 in darker red, while residues with a score between 0.5 and 0.4 in lighter red. The structures of the corresponding E. coli proteins (PDB: 2NWC for GroEL, 2KHO for DnaK and 1QVC for SSB) are also depicted in light grey with the conserved disordered segments marked by red or added as red dashed lines. In the heptameric GroEL and tetrameric SSB structures one chain is depicted by darker grey than the others
Mentions: Interestingly, chaperones seem to rely on structural disorder the most. For example, the C-terminal tail of GroEL preserved its disordered nature in most minimal and reference species (Fig. 1a). Although the E. coli sequence is not predicted as disordered, this is certainly a misprediction because the respective region is missing from available X-ray structures (Fig. 1a). The highly flexible, hydrophilic tails protrude into the cavity of the ball-shaped chaperonin cage formed by GroEL/GroES subunits and assist the correct folding of proteins [36]. Multiple studies collectively confirmed that truncation of the tail impairs the efficient refolding of substrate proteins [36–39], however its specific molecular role in the chaperonin reaction cycle is still under debate [38, 39].Fig. 1

View Article: PubMed Central - PubMed

ABSTRACT

Abstract: Intrinsically disordered regions (IDRs) of proteins fulfill important regulatory roles in most organisms. However, the proteins of certain endosymbiont and intracellular pathogenic bacteria with extremely reduced genomes contain disproportionately small amounts of IDRs, consisting almost entirely of folded domains. As their genomes co-evolving with their hosts have been reduced in unrelated lineages, the proteomes of these bacteria represent independently evolved minimal protein sets. We systematically analyzed structural disorder in a representative set of such minimal organisms to see which types of functionally relevant longer IDRs are invariably retained in them. We found that a few characteristic functions are consistently linked with conformational disorder: ribosomal proteins, key components of the protein production machinery, a central coordinator of DNA metabolism and certain housekeeping chaperones seem to strictly rely on structural disorder even in genome-reduced organisms. We propose that these functions correspond to the most essential and probably also the most ancient ones fulfilled by structural disorder in cellular organisms.

Reviewers: This article was reviewed by Michael Gromiha, Zoltan Gaspari and Sandor Pongor.

Electronic supplementary material: The online version of this article (doi:10.1186/s13062-016-0149-y) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus