Ribonucleotide reduction - horizontal transfer of a required function spans all three domains

BMC Evolutionary Biology

Research Article

Britt-Marie Sjöberg¹  Daniel Lundin¹  Eduard Torrents²  Anthony M Poole³  Simonetta Gribaldo⁴ 

[1] Department of Molecular Biology and Functional Genomics, Stockholm University, SE-106 91, Stockholm, Sweden;Department of Molecular Biology and Functional Genomics, Stockholm University, SE-106 91, Stockholm, Sweden;Institute for Bioengineering of Catalonia (IBEC), Scientific Park of Barcelona, Barcelona, Spain;Department of Molecular Biology and Functional Genomics, Stockholm University, SE-106 91, Stockholm, Sweden;School of Biological Sciences, University of Canterbury, 8140, Christchurch, New Zealand;Unite Biologie Moléculaire du Gène chez les Extremophiles (BMGE), Departement de Microbiologie, Institut Pasteur, Paris, France;

关键词: Horizontal Gene Transfer;    Ribonucleotide Reductase;    Horizontal Gene Transfer Event;    Archaeal Sequence;    Last Eukaryotic Common Ancestor;   

DOI  :  10.1186/1471-2148-10-383

 received in 2010-09-27, accepted in 2010-12-10,  发布年份 2010

来源: Springer

【 摘 要 】

BackgroundRibonucleotide reduction is the only de novo pathway for synthesis of deoxyribonucleotides, the building blocks of DNA. The reaction is catalysed by ribonucleotide reductases (RNRs), an ancient enzyme family comprised of three classes. Each class has distinct operational constraints, and are broadly distributed across organisms from all three domains, though few class I RNRs have been identified in archaeal genomes, and classes II and III likewise appear rare across eukaryotes. In this study, we examine whether this distribution is best explained by presence of all three classes in the Last Universal Common Ancestor (LUCA), or by horizontal gene transfer (HGT) of RNR genes. We also examine to what extent environmental factors may have impacted the distribution of RNR classes.ResultsOur phylogenies show that the Last Eukaryotic Common Ancestor (LECA) possessed a class I RNR, but that the eukaryotic class I enzymes are not directly descended from class I RNRs in Archaea. Instead, our results indicate that archaeal class I RNR genes have been independently transferred from bacteria on two occasions. While LECA possessed a class I RNR, our trees indicate that this is ultimately bacterial in origin. We also find convincing evidence that eukaryotic class I RNR has been transferred to the Bacteroidetes, providing a stunning example of HGT from eukaryotes back to Bacteria. Based on our phylogenies and available genetic and genomic evidence, class II and III RNRs in eukaryotes also appear to have been transferred from Bacteria, with subsequent within-domain transfer between distantly-related eukaryotes. Under the three-domains hypothesis the RNR present in the last common ancestor of Archaea and eukaryotes appears, through a process of elimination, to have been a dimeric class II RNR, though limited sampling of eukaryotes precludes a firm conclusion as the data may be equally well accounted for by HGT.ConclusionsHorizontal gene transfer has clearly played an important role in the evolution of the RNR repertoire of organisms from all three domains of life. Our results clearly show that class I RNRs have spread to Archaea and eukaryotes via transfers from the bacterial domain, indicating that class I likely evolved in the Bacteria. However, against the backdrop of ongoing transfers, it is harder to establish whether class II or III RNRs were present in the LUCA, despite the fact that ribonucleotide reduction is an essential cellular reaction and was pivotal to the transition from RNA to DNA genomes. Instead, a general pattern of ongoing horizontal transmission emerges wherein environmental and enzyme operational constraints, especially the presence or absence of oxygen, are likely to be major determinants of the RNR repertoire of genomes.

【 授权许可】

Unknown   
© Lundin et al; licensee BioMed Central Ltd. 2010. This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.