NORMAL GENOMIC

• Brindefalk B, Viklund J, Larsson D, Thollesson M, Andersson SG
• Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases.
• Mol Biol Evol. 2007; 24: 743-56
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• Many theories favor a fusion of 2 prokaryotic genomes for the origin ofthe Eukaryotes, but there are disagreements on the origin, timing, andcellular structures of the cells involved. Equally controversial is thesource of the nuclear genes for mitochondrial proteins, although thealpha-proteobacterial contribution to the mitochondrial genome is wellestablished. Phylogenetic inferences show that the nuclearly encodedmitochondrial aminoacyl-tRNA synthetases (aaRSs) occupy a position in thetree that is not close to any of the currently sequencedalpha-proteobacterial genomes, despite cohesive and remarkablywell-resolved alpha-proteobacterial clades in 12 of the 20 trees. Two ormore alpha-proteobacterial clusters were observed in 8 cases, indicativeof differential loss of paralogous genes or horizontal gene transfer.Replacement and retargeting events within the nuclear genomes of theEukaryotes was indicated in 10 trees, 4 of which also show splitalpha-proteobacterial groups. A majority of the mitochondrial aaRSsoriginate from within the bacterial domain, but none specifically from thealpha-Proteobacteria. For some aaRS, the endosymbiotic origin may havebeen erased by ongoing gene replacements on the bacterial as well as theeukaryotic side. For others that accurately resolve thealpha-proteobacterial divergence patterns, the lack of affiliation withmitochondria is more surprising. We hypothesize that the ancestraleukaryotic gene pool hosted primordial "bacterial-like" genes, to which alimited set of alpha-proteobacterial genes, mostly coding for componentsof the respiratory chain complexes, were added and selectively maintained.

• Shaul S, Nussinov R, Pupko T
• Paths of lateral gene transfer of lysyl-aminoacyl-tRNA synthetases with aunique evolutionary transition stage of prokaryotes coding for class I andII varieties by the same organisms.
• BMC Evol Biol. 2006; 6: 22-22
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• BACKGROUND: While the premise that lateral gene transfer (LGT) is adominant evolutionary force is still in considerable dispute, the case forwidespread LGT in the family of aminoacyl-tRNA synthetases (aaRS) is nolonger contentious. aaRSs are ancient enzymes, guarding the fidelity ofthe genetic code. They are clustered in two structurally unrelatedclasses. Only lysine aminoacyl-tRNA synthetase (LysRS) is found both as aclass 1 and a class 2 enzyme (LysRS1-2). Remarkably, in several extantprokaryotes both classes of the enzyme coexist, a unique phenomenon thathas yet to receive its due attention. RESULTS: We applied a phylogeneticapproach for determining the extent and origin of LGT in prokaryoticLysRS. Reconstructing species trees for Archaea and Bacteria, andinferring that their last common ancestors encoded LysRS1 and LysRS2,respectively, we studied the gains and losses of both classes. A complexpattern of LGT events emerged. In specific groups of organisms LysRS1 wasreplaced by LysRS2 (and vice versa). In one occasion, within the alphaproteobacteria, a LysRS2 to LysRS1 LGT was followed by reversal to LysRS2.After establishing the most likely LGT paths, we studied the possibleorigins of the laterally transferred genes. To this end, we reconstructedLysRS gene trees and evaluated the likely origins of the laterallytransferred genes. While the sources of LysRS1 LGTs were readilyidentified, those for LysRS2 remain, for now, uncertain. The replacementof one LysRS by another apparently transits through a stage simultaneouslycoding for both synthetases, probably conferring a selective advantage tothe affected organisms. CONCLUSION: The family of LysRSs features complexLGT events. The currently available data were sufficient for identifyingunambiguously the origins of LysRS1 but not of LysRS2 gene transfers. Aselective advantage is suggested to organisms encoding simultaneouslyLysRS1-2.

• Andersson JO, Sarchfield SW, Roger AJ
• Gene transfers from nanoarchaeota to an ancestor of diplomonads andparabasalids.
• Mol Biol Evol. 2005; 22: 85-90
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• Rare evolutionary events, such as lateral gene transfers and gene fusions,may be useful to pinpoint, and correlate the timing of, key branchesacross the tree of life. For example, the shared possession of atransferred gene indicates a phylogenetic relationship among organismallineages by virtue of their shared common ancestral recipient. Here, wepresent phylogenetic analyses of prolyl-tRNA and alanyl-tRNA synthetasegenes that indicate lateral gene transfer events to an ancestor of thediplomonads and parabasalids from lineages more closely related to thenewly discovered archaeal hyperthermophile Nanoarchaeum equitans(Nanoarchaeota) than to Crenarchaeota or Euryarchaeota. The support forthis scenario is strong from all applied phylogenetic methods for thealanyl-tRNA sequences, whereas the phylogenetic analyses of theprolyl-tRNA sequences show some disagreements between methods, indicatingthat the donor lineage cannot be identified with a high degree ofcertainty. However, in both trees, the diplomonads and parabasalids branchtogether within the Archaea, strongly suggesting that these two groups ofunicellular eukaryotes, often regarded as the two earliest independentoffshoots of the eukaryotic lineage, share a common ancestor to theexclusion of the eukaryotic root. Unfortunately, the phylogenetic analysesof these two aminoacyl-tRNA synthetase genes are inconclusive regardingthe position of the diplomonad/parabasalid group within the eukaryotes.Our results also show that the lineage leading to Nanoarchaeota branchedoff from Euryarchaeota and Crenarchaeota before the divergence ofdiplomonads and parabasalids, that this unexplored archaeal diversity,currently only represented by the hyperthermophilic organism Nanoarchaeumequitans, may include members living in close proximity to mesophiliceukaryotes, and that the presence of split genes in the Nanoarchaeumgenome is a derived feature.

• Iyer LM, Koonin EV, Aravind L
• Evolution of bacterial RNA polymerase: implications for large-scalebacterial phylogeny, domain accretion, and horizontal gene transfer.
• Gene. 2004; 335: 73-88
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• Comparative analysis of the domain architectures of the beta, beta', andsigma(70) subunits of bacterial DNA-dependent RNA polymerases (DdRp),combined with sequence-based phylogenetic analysis, revealed a fundamentalsplit among bacteria. DNA-dependent RNA polymerase subunits of Group I,which includes Proteobacteria, Aquifex, Chlamydia, Spirochaetes,Cytophaga-Chlorobium, and Planctomycetes, are characterized by threedistinct inserts, namely a Sandwich Barrel Hybrid Motif domain in the betasubunit, a beta-beta' module (BBM) 1 domain in the beta' subunit, and adistinct helical module in the sigma subunit. The DdRp subunits ofremaining bacteria, which comprise Group II, lack these inserts, althoughsome additional inserted domains are present in individual lineages. Theseparation of bacteria into Group I and Group II is generally compatiblewith the topologies of phylogenetic trees of the conserved regions of DdRpsubunits and concatenated ribosomal proteins and might represent theprimary bifurcation in bacterial evolution. A striking deviation from thisevolutionary pattern is Aquifex whose DdRp subunits cluster within GroupI, whereas phylogenetic analysis of ribosomal proteins identifies Aquifexas grouping with Thermotoga another bacterial hyperthemophile belonging toGroup II. The inferred evolutionary scenario for the DdRp subunitsincludes domain accretion and rearrangement, with some likely horizontaltransfer events. Although evolution of bacterial DdRp appeared to begenerally dominated by vertical inheritance, horizontal transfer ofcomplete genes for all or some of the subunits, resulting in displacementof the ancestral genes, might have played a role in several lineages, suchas Aquifex, Thermotoga, and Fusobacterium.

• Aravind L, Anantharaman V, Koonin EV
• Monophyly of class I aminoacyl tRNA synthetase, USPA, ETFP, photolyase,and PP-ATPase nucleotide-binding domains: implications for proteinevolution in the RNA.
• Proteins. 2002; 48: 1-14
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• Protein sequence and structure comparisons show that the catalytic domainsof Class I aminoacyl-tRNA synthetases, a related family ofnucleotidyltransferases involved primarily in coenzyme biosynthesis,nucleotide-binding domains related to the UspA protein (USPA domains),photolyases, electron transport flavoproteins, and PP-loop-containingATPases together comprise a distinct class of alpha/beta domainsdesignated the HUP domain after HIGH-signature proteins, UspA, andPP-ATPase. Several lines of evidence are presented to support themonophyly of the HUP domains, to the exclusion of other three-layeredalpha/beta folds with the generic "Rossmann-like" topology. Cladisticanalysis, with patterns of structural and sequence similarity used asdiscrete characters, identified three major evolutionary lineages withinthe HUP domain class: the PP-ATPases; the HIGH superfamily, which includesclass I aaRS and related nucleotidyltransferases containing the HIGHsignature in their nucleotide-binding loop; and a previously unrecognizedUSPA-like group, which includes USPA domains, electron transportflavoproteins, and photolyases. Examination of the patterns of phyleticdistribution of distinct families within these three major lineagessuggests that the Last Universal Common Ancestor of all modern life formsencoded 15-18 distinct alpha/beta ATPases and nucleotide-binding proteinsof the HUP class. This points to an extensive radiation of HUP domainsbefore the last universal common ancestor (LUCA), during which themultiple class I aminoacyl-tRNA synthetases emerged only at a late stage.Thus, substantial evolutionary diversification of protein domains occurredwell before the modern version of the protein-dependent translationmachinery was established, i.e., still in the RNA world.

• Wolf YI, Rogozin IB, Grishin NV, Tatusov RL, Koonin EV
• Genome trees constructed using five different approaches suggest new majorbacterial clades.
• BMC Evol Biol. 2001; 1: 8-8
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• BACKGROUND: The availability of multiple complete genome sequences fromdiverse taxa prompts the development of new phylogenetic approaches, whichattempt to incorporate information derived from comparative analysis ofcomplete gene sets or large subsets thereof. Such attempts areparticularly relevant because of the major role of horizontal genetransfer and lineage-specific gene loss, at least in the evolution ofprokaryotes. RESULTS: Five largely independent approaches were employed toconstruct trees for completely sequenced bacterial and archaeal genomes:i) presence-absence of genomes in clusters of orthologous genes; ii)conservation of local gene order (gene pairs) among prokaryotic genomes;iii) parameters of identity distribution for probable orthologs; iv)analysis of concatenated alignments of ribosomal proteins; v) comparisonof trees constructed for multiple protein families. All constructed treessupport the separation of the two primary prokaryotic domains, bacteriaand archaea, as well as some terminal bifurcations within the bacterialand archaeal domains. Beyond these obvious groupings, the trees made withdifferent methods appeared to differ substantially in terms of therelative contributions of phylogenetic relationships and similarities ingene repertoires caused by similar life styles and horizontal genetransfer to the tree topology. The trees based on presence-absence ofgenomes in orthologous clusters and the trees based on conserved genepairs appear to be strongly affected by gene loss and horizontal genetransfer. The trees based on identity distributions for orthologs andparticularly the tree made of concatenated ribosomal protein sequencesseemed to carry a stronger phylogenetic signal. The latter tree supportedthree potential high-level bacterial clades,: i) Chlamydia-Spirochetes,ii) Thermotogales-Aquificales (bacterial hyperthermophiles), and ii)Actinomycetes-Deinococcales-Cyanobacteria. The latter group also appearedto join the low-GC Gram-positive bacteria at a deeper tree node. These newgroupings of bacteria were supported by the analysis of alternativetopologies in the concatenated ribosomal protein tree using theKishino-Hasegawa test and by a census of the topologies of 132 individualgroups of orthologous proteins. Additionally, the results of this analysisput into question the sister-group relationship between the two majorarchaeal groups, Euryarchaeota and Crenarchaeota, and suggest instead thatEuryarchaeota might be a paraphyletic group with respect to Crenarchaeota.CONCLUSIONS: We conclude that, the extensive horizontal gene flow andlineage-specific gene loss notwithstanding, extension of phylogeneticanalysis to the genome scale has the potential of uncovering deepevolutionary relationships between prokaryotic lineages.

• Woese CR, Olsen GJ, Ibba M, Soll D
• Aminoacyl-tRNA synthetases, the genetic code, and the evolutionaryprocess.
• Microbiol Mol Biol Rev. 2000; 64: 202-36
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• The aminoacyl-tRNA synthetases (AARSs) and their relationship to thegenetic code are examined from the evolutionary perspective. Despite aloose correlation between codon assignments and AARS evolutionaryrelationships, the code is far too highly structured to have been orderedmerely through the evolutionary wanderings of these enzymes. Nevertheless,the AARSs are very informative about the evolutionary process. Examinationof the phylogenetic trees for each of the AARSs reveals the following. (i)Their evolutionary relationships mostly conform to established organismalphylogeny: a strong distinction exists between bacterial- andarchaeal-type AARSs. (ii) Although the evolutionary profiles of theindividual AARSs might be expected to be similar in general respects, theyare not. It is argued that these differences in profiles reflect thestages in the evolutionary process when the taxonomic distributions of theindividual AARSs became fixed, not the nature of the individual enzymes.(iii) Horizontal transfer of AARS genes between Bacteria and Archaea isasymmetric: transfer of archaeal AARSs to the Bacteria is more prevalentthan the reverse, which is seen only for the "gemini group. " (iv) Themost far-ranging transfers of AARS genes have tended to occur in thedistant evolutionary past, before or during formation of the primaryorganismal domains. These findings are also used to refine the theory thatat the evolutionary stage represented by the root of the universalphylogenetic tree, cells were far more primitive than their moderncounterparts and thus exchanged genetic material in far less restrictedways, in effect evolving in a communal sense.

• Diaz-Lazcoz Y, Aude JC, Nitschke P, Chiapello H, Landes-Devauchelle C, Risler JL
• Evolution of genes, evolution of species: the case of aminoacyl-tRNAsynthetases.
• Mol Biol Evol. 1998; 15: 1548-61
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• All of the aminoacyl-tRNA synthetase (aaRS) sequences currently availablein the data banks have been subjected to a systematic analysis aimed atfinding gene duplications, genetic recombinations, and horizontaltransfers. Evidence is provided for the occurrence (or probableoccurrence) of such phenomena within this class of enzymes. In particular,it is suggested that the monomeric PheRS from the yeast mitochondrion is achimera of the alpha and beta chains of the standard tetrameric protein.In addition, it is proposed that the dimeric and tetrameric forms of GlyRSare the result of a double and independent acquisition of the samespecificity within two different subclasses of aaRS. The phylogeneticreconstructions of the evolutionary histories of the genes encoding aaRSare shown to be extremely diverse. While large segments of the populationare consistent with the broad grouping into the three Woesian domains,some phylogenetic reconstructions do not place the Archae and the Eucaryaas sister groups but, rather, show a gram-negative bacteria/eukaryoteclustering. In addition, many individual genes pose difficulties thatpreclude any simple evolutionary scheme. Thus, aaRS's are clearly aparadigm of F. Jacob's "odd jobs of evolution" but, on the whole, do notcall into question the evolutionary scenario originally proposed by Woeseand subsequently refined by others.