Analysis of the distribution and evolution of the <scp>ATP</scp>‐dependent <scp>DNA</scp> ligases of bacteria delineates a distinct phylogenetic group ‘<scp>L</scp>ig <scp>E</scp>’

Williamson, Adele Kim; Hjerde, Erik; Kahlke, Tim

doi:10.1111/mmi.13229

Cited by 17 publications

(57 citation statements)

References 70 publications

(120 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This analogous sequence context indicates that AD-Lig P has genetically substituted the ND-ligase in high-light strains, and suggests it may also functionally replace it in DNA replication. As we have previously described, AD-Lig P is active on singly nicked or cohesive breaks and prefers Mg as a divalent cation (4,7). We further confirmed the predicted cofactor preferences of ND-Lig fl and AD-Lig P as NAD and ATP by assaying purified recombinant protein ( Fig 1E).…”

Section: Resultssupporting

confidence: 88%

“…DNA ligases were identified in all genomes by searching for the nucleotidyltransferase domain of ND-ligases (PF01653) and AD-ligases (PF01068). Fulllength coding sequences were retrieved and additional ligase-associated domains detected using Pfam as described previously (4). Whole genome alignments were constructed using progressiveMAUVE with default settings (12).…”

Section: Methodsmentioning

confidence: 99%

“…This key difference in cellular replication machinery represents a central delineation between bacterial and archaeal/eukaryotic cell lineages (2); however the reason why bacteria preferentially use of NAD-ligases remains a long-standing question in the field (3). Previously, we described how strains of the marine cyanobacterium Prochlorococcus marinus encode multiple AD-ligases in their genomes, yet lack the other subunits associated with known AD-ligase-dependent repair pathways (4). P. marinus ecotypes are broadly classified as high-light which reside in the UV-damaging nutrient-poor upper ocean and low-light which experience less UV, and have higher nutrient access (5).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

DNA ligases of Prochlorococcus marinus: an evolutionary exception to the rules of replication

Hjerde

Maguren

Rzoska-Smith

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

DNA ligases, essential enzymes which re-join the backbone of DNA come in two structurallydistinct isoforms, NAD-dependent and ATP-dependent, which differ in cofactor usage. The present view is that all bacteria exclusively use NAD-dependent DNA ligases for DNA replication, while archaea and eukaryotes use ATP-dependent DNA ligases. Some bacteria also possess auxiliary ATP-dependent DNA ligases; however, these are only employed for specialist DNA repair processes. Here we show that in the genomes of high-light strains of the marine cyanobacterium Prochlorococcocus marinus, an ATP-dependent DNA ligase has replaced the NAD-dependent form, overturning the present paradigm of a clear evolutionary split in ligase usage. Genes encoding partial NAD-dependent DNA ligases are found on mobile regions in highlight genomes and lack domains required for catalytic function. This constitutes the first reported example of a bacterium that relies on an ATP-dependent DNA ligase for DNA replication and recommends P. marinus as a model to investigate the evolutionary origins of these essential DNA-processing enzymes.

show abstract

Section: Resultssupporting

confidence: 88%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

DNA ligases of Prochlorococcus marinus: an evolutionary exception to the rules of replication

Hjerde

Maguren

Rzoska-Smith

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…One difficulty in such comparative analyses is distinguishing between substitutions imparting psychrophilicity and those that have occurred through genetic drift. To exclude possible false-positive findings based on phylogenetic resemblance, we included Lig E from V. cholera in our sequence comparison as previous phylogenomic studies have placed this close to Vib-Lig in evolutionary terms (Williamson et al 2016), thus representing a genus-related but mesophilic organism. Coming from a mesophilic human pathogen, Vch-Lig is not anticipated to exhibit cold-adapted characteristics.…”

Section: Discussionmentioning

confidence: 99%

Temperature adaptation of DNA ligases from psychrophilic organisms

2019

Self Cite

View full text Add to dashboard Cite

DNA ligases operating at low temperatures have potential advantages for use in biotechnological applications. For this reason, we have characterised the temperature-optima and thermal stabilities of three minimal Lig E-type ATP-dependant DNA ligase originating from Gram-negative obligate psychrophilic bacteria. The three ligases, denoted Vib-Lig, Psy-Lig and Par-Lig show a remarkable range of thermal stabilities and optima, with the first bearing all the hallmarks of a genuinely coldadapted enzyme, while the latter two have activity and stability profiles more typical of mesophilic proteins. A comparative approach based on sequence comparison and homology modelling indicates that the cold-adapted features of Vib-Lig may be ascribed to differences in surface charge rather than increased local or global flexibility: which is consistent with the contemporary emerging paradigm of the physical basis of cold adaptation of enzymes.

show abstract

“…The minimal Lig E-type DNA ligases comprise a clade of phylogenetically distinct ATP-dependent DNA ligases found almost exclusively in proteobacteria ( 10 ). The majority of these enzymes lack any appending domains and possess a predicted N-terminal signal sequence for localization in the periplasm, the removal of which increases both protein stability and activity ( 11 ).…”

Section: Introductionmentioning

confidence: 99%

DNA binding with a minimal scaffold: structure–function analysis of Lig E DNA ligases

Williamson

Grgić

Leiros

2018

Nucleic Acids Research

Self Cite

View full text Add to dashboard Cite

DNA ligases join breaks in the phosphodiester backbone of DNA by catalysing the formation of bonds between opposing 5′P and 3′OH ends in an adenylation-dependent manner. Catalysis is accompanied by reorientation of two core domains to provide access to the active site for cofactor utilization and enable substrate binding and product release. The general paradigm is that DNA ligases engage their DNA substrate through complete encirclement of the duplex, completed by inter-domain kissing contacts via loops or additional domains. The recent structure of a minimal Lig E-type DNA ligase, however, implies it must use a different mechanism, as it lacks any domains or loops appending the catalytic core which could complete encirclement. In the present study, we have used a structure-guided mutagenesis approach to investigate the role of conserved regions in the Lig E proteins with respect to DNA binding. We report the structure of a Lig-E type DNA ligase bound to the nicked DNA-adenylate reaction intermediate, confirming that complete encirclement is unnecessary for substrate engagement. Biochemical and biophysical measurements of point mutants to residues implicated in binding highlight the importance of basic residues in the OB domain, and inter-domain contacts to the linker.

show abstract

Analysis of the distribution and evolution of the ATP‐dependent DNA ligases of bacteria delineates a distinct phylogenetic group ‘Lig E’

Cited by 17 publications

References 70 publications

DNA ligases of Prochlorococcus marinus: an evolutionary exception to the rules of replication

DNA ligases of Prochlorococcus marinus: an evolutionary exception to the rules of replication

Temperature adaptation of DNA ligases from psychrophilic organisms

DNA binding with a minimal scaffold: structure–function analysis of Lig E DNA ligases

Contact Info

Product

Resources

About