Structural and evolutionary analyses reveal determinants of DNA binding specificities of nucleoid-associated proteins HU and IHF

Dey, Debayan; Nagaraja, Valakunja; Ramakumar, Suryanarayanarao

doi:10.1016/j.ympev.2016.11.014

Cited by 35 publications

(44 citation statements)

References 55 publications

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“…Multiple sequence alignment (MSA) was performed by the rate matrix of residue substitution search using an algorithm described in supporting materials ( S1 File ) and the Clustal program from UniProt Consortium tools [ 1 ]. All HU/IHF sequences were aligned with only exception of Bacteroidetes phylum, where just a half of HU/IHF family proteins sequences gives good MSA [ 2 ]. These proteins were further analyzed while phylum Bacteroidetes HU/IHF family proteins which have poor MSA were excluded from further analysis.…”

Section: Methodsmentioning

confidence: 99%

“…The HU/IHF family of proteins (also referred to Type II DNA-binding proteins) consists of orthologs that share significant sequence homology [ 31 ]. Protein sequence alignment and clusterization as well as phylogenetic analysis of thousands HU/IHF proteins, which sequences are available, were performed to identify their taxonomic position, evolutionary connections with other protein families and functionally important structural motives [ 2 ]. Search for key amino acids that determine DNA binding properties of HU/IHF proteins is also attractive: HU and IHF sequence comparison suggests key residues for the IHF DNA recognition [ 2 , 36 ].…”

Section: Introductionmentioning

confidence: 99%

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Comparison of histone-like HU protein DNA-binding properties and HU/IHF protein sequence alignment

et al. 2017

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BackgroundThe structure and function of bacterial nucleoid are controlled by histone-like proteins of HU/IHF family, omnipresent in bacteria and also founding archaea and some eukaryotes.HU protein binds dsDNA without sequence specificity and avidly binds DNA structures with propensity to be inclined such as forks, three/four-way junctions, nicks, overhangs and DNA bulges. Sequence comparison of thousands of known histone-like proteins from diverse bacteria phyla reveals relation between HU/IHF sequence, DNA–binding properties and other protein features.Methodology and principal findingsPerformed alignment and clusterization of the protein sequences show that HU/IHF family proteins can be unambiguously divided into three groups, HU proteins, IHF_A and IHF_B proteins. HU proteins, IHF_A and IHF_B proteins are further partitioned into several clades for IHF and HU; such a subdivision is in good agreement with bacterial taxonomy. We also analyzed a hundred of 3D fold comparative models built for HU sequences from all revealed HU clades. It appears that HU fold remains similar in spite of the HU sequence variations. We studied DNA–binding properties of HU from N. gonorrhoeae, which sequence is similar to one of E.coli HU, and HU from M. gallisepticum and S. melliferum which sequences are distant from E.coli protein. We found that in respect to dsDNA binding, only S. melliferum HU essentially differs from E.coli HU. In respect to binding of distorted DNA structures, S. melliferum HU and E.coli HU have similar properties but essentially different from M. gallisepticum HU and N. gonorrhea HU. We found that in respect to dsDNA binding, only S. melliferum HU binds DNA in non-cooperative manner and both mycoplasma HU bend dsDNA stronger than E.coli and N. gonorrhoeae. In respect to binding to distorted DNA structures, each HU protein has its individual profile of affinities to various DNA-structures with the increased specificity to DNA junction.Conclusions and significanceHU/IHF family proteins sequence alignment and classification are updated. Comparative modeling demonstrates that HU protein 3D folding’s even more conservative than HU sequence. For the first time, DNA binding characteristics of HU from N. gonorrhoeae, M. gallisepticum and S. melliferum are studied. Here we provide detailed analysis of the similarity and variability of DNA-recognizing and bending of four HU proteins from closely and distantly related HU clades.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Comparison of histone-like HU protein DNA-binding properties and HU/IHF protein sequence alignment

et al. 2017

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“…Accordingly, we initiated iterative PSI-BLAST 43 and JACKHMMER 44 searches against a curated database of 6430 complete proteomes drawn from across the tree of life. In addition to the major HU and IHF clades, these searches detected with significant e-values several divergent versions in bacteria, especially from the bacteroidetes-chlorobi lineage, which is known to possess multiple paralogs of this superfamily 26 . While these have not been comprehensively sampled in previous studies, our searches enabled us to obtain a comprehensive collection of all members of the superfamily from this lineage, including several divergent ones.…”

Section: Resultsmentioning

confidence: 95%

“…The dramatic but poorly understood lineage-specific expansion of HU domains 26 and the unusual structural modification of the HU-CCDC81 domain, which emerged in the bacteroidetes lineage, prompted us to more closely examine the evolutionary radiation and functional diversification of the HU superfamily in this lineage. Our phylogenetic analysis revealed that in bacteroidetes, the HU superfamily shows 2 distinct clades beyond the HU-CCDC81 clade (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Novel clades of the HU/IHF superfamily point to unexpected roles in the eukaryotic centrosome, chromosome partitioning, and biologic conflicts

et al. 2017

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The HU superfamily of proteins, with a unique DNA-binding mode, has been extensively studied as the primary chromosome-packaging protein of the bacterial superkingdom. Representatives also play a role in DNA-structuring during recombination events and in eukaryotic organellar genome maintenance. However, beyond these well-studied roles, little is understood of the functional diversification of this large superfamily. Using sensitive sequence and structure analysis methods we identify multiple novel clades of the HU superfamily. We present evidence that a novel eukaryotic clade prototyped by the human CCDC81 protein acquired roles beyond DNA-binding, likely in protein-protein interaction in centrosome organization and as a potential cargo-binding protein in conjunction with Dynein-VII. We also show that these eukaryotic versions were acquired via an early lateral transfer from bacteroidetes, where we predict a role in chromosome partition. This likely happened before the last eukaryotic common ancestor, pointing to potential endosymbiont contributions beyond that of the mitochondrial progenitor. Further, we show that the dramatic lineage-specific expansion of this domain in the bacteroidetes lineage primarily is linked to a functional shift related to potential recognition and preemption of genome invasive entities such as mobile elements. Remarkably, the CCDC81 clade has undergone a similar massive lineage-specific expansion within the archosaurian lineage in birds, suggesting a possible use of the HU superfamily in a similar capacity in recognition of non-self molecules even in this case.

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2020

Structure and Function of the Bacterial Genome

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Structural and evolutionary analyses reveal determinants of DNA binding specificities of nucleoid-associated proteins HU and IHF

Cited by 35 publications

References 55 publications

Comparison of histone-like HU protein DNA-binding properties and HU/IHF protein sequence alignment

Comparison of histone-like HU protein DNA-binding properties and HU/IHF protein sequence alignment

Novel clades of the HU/IHF superfamily point to unexpected roles in the eukaryotic centrosome, chromosome partitioning, and biologic conflicts

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