Descent of Bacteria and Eukarya from an archaeal root of life

Abstract

17The three biological domains delineated based on SSU rRNAs are confronted by 18 uncertainties regarding the relationship between Archaea and Bacteria, and the origin of 19Eukarya. Herein the homologies between the paralogous valyl-tRNA and isoleucyl-tRNA 20 synthetases in a wide spectrum of species revealed vertical gene transmission from an 21 archaeal root of life through a Primitive Archaea Cluster to an Ancestral Bacteria Cluster of 22Molecular evolution analysis of small subunit ribosomal RNA (SSU rRNA) yielded a 32 universal but unrooted tree of life (ToL) that comprises the three biological domains of 33 Archaea, Bacteria and Eukarya 1 . A ToL of transfer RNAs based on the genetic distances 34 between the 20 classes of tRNA acceptors for different amino acids located its root near the 35 hyperthermophilic archaeal methanogen Methanopyrus (Mka) 2 . Although this rooting is 36 supported by a wide range of evidence 3-9 , and the age of ~2.7 Gya for the Methanopyrus 37 lineage as the oldest among living organisms 10 , the phylogenies of the three biological 38 domains are beset by two fundamental problems: viz. the uncertain relationship between 39Archaea and Bacteria, and the identity of the prokaryotic-parent that underwent genome 40 merger with an alphaproteobacterium to give rise to Eukarya. As long as these two problems 41 remain unresolved, the nature of the root of life is open to diverse formulations [11][12][13][14][15] . 42Accordingly, the objective of the present study is to examine the pathways of descent of 43 Bacteria and Eukarya from an archaeal root of life, and the nature of the archaeal-parent of 44Eukarya. 45 46The antiquity of proteins could be assessed based on the increasing divergence of paralogous 47 proteins in time 16 . Applying this approach, BLASTP was performed between the intraspecies 48 valyl-tRNA synthetase (VARS) and isoleucyl-tRNA synthetase (IARS) in the genomic 49 sequences for 5,398 species in NCBI Genbank. Arrangement of the BLASTP bitscores 50 obtained in descending order ( Supplementary Table S1 and partly in Fig. 1) showed that the 51 119 highest scoring species were all archaeons, topped by Mka and including Mfe, Afu, Mnt 52and Mja with bitscores of 473, 436, 387, 387 and 387 respectively. The top scoring bacterium 53 was the Clostridium Mau with a bit score of 378, and the top scoring eukaryote was the 54 filamentous brown alga Esi with a bit score of 240. These results established the foremost 55 antiquity of Mka among extant organisms. 56

An ectosymbiosis-based mechanism of eukaryogenesis

“…The NGDAWV-motif was found in not only the alphaproteobacteria Tis, Atu and Rru, but also the gammaproteobacterium Eco and the deltaproteobacterium Pel. Such diversified motifs in both AMIs and MTEs were in keeping with the profuse variety of prokaryotic proteins found in the proteomes of eukaryotes 8,24–27 , but neither the diversity nor the apparent paucity or lack of the EKP motif in the MTEs was consistent with the origin of all MTE and AMI Hsp70s from a single alphaproteobacterial endosymbiont.…”

“…The entry of prokaryotic proteins into eukaryotes could be mediated by a number of different mechanisms. While horizontal gene transfers (HGTs) might be limited by low rates of acceptance by the gene recipients 33 , it was found recently that some archaea displayed an ‘accelerated gene adoption’ (AGA) phenotype detectible by the elevated levels of bacteria-derived proteins in their proteomes 8 . Moreover, the genes of the bacterial species Rpr, Bap, Ctr, Mpn, and Tpa furnished relatively few protein coding genes that were adopted by the AGA-active archaeons, and their proteins were also depleted in the proteomes of both Gla and Trv, demonstrating the key role played by AGA in controlling influx of bacterial genes into the eukaryogenic lineage.…”

“…Also the paucity of AGA activity in bacteria would also render them much less effective than archaea in hosting eukaryogenesis owing to the importance of collection of exogenous genes by the host in this regard. Anaerobic Abo and its facultatively anaerobic companion species Acf, on account of their top average similarity bitscores among archaeons toward Gla and Trv proteomes and the PEP-utilizing enzyme mobile domain of Gla, along with their outstanding AGA activity, emerged as leading candidate archaeal parents 8 . When the DNA-biology enzymes/proteins belonging to the Cluster of Ortholog Groups (COG) for replication, recombination and repair 34 were analyzed with respect to the similarity bitscores displayed by primitive AMIs toward Abo and various Asgard and TACK archaeons which included some attractive candidate archaeal parents 8,35 ,the frequencies of top similarity bitscores received by Abo from the primitive AMIs pertaining to the DNA-biology enzymes, viz.…”

“…However, the discoveries of typical mitochondrial proteins in the AMIs gave rise to the ‘endosymbiosis first’ theory that the presence of mitochondrial proteins in AMIs implies the harboring of mitochondria or their endosymbiotic ancestors by the AMIs in the past 5,6 . As a result, the proposal of Lokiarchaeota being a suitable archaeal parent was held up by the missing mechanism for importing an alphaproteobacterial endosymbiont 7 , and the proposal of the Aciduliprofundum archaeons being appropriate archaeal parents would not be implementable if these small archaeons are required to accommodate an upfront endosymbiont 8 . In addition, searches have not yielded a consensual phylogenetic location for the Last Eukaryotic Common Ancestor (LECA) 9–12 , and autogenous development of eukaryotes has not given a better fit to omics data than endosymbiosis 13 .…”

Chaos, Order and Systematics in Evolution of the Genetic Code

“…Based on our analyses and those of others, we consider Archaea to be most similar to LUCA and Bacteria to be more diverged. The third major transition is the genetic fusion of multiple Archaea and multiple Bacteria to generate Eukaryota [22][23][24][25]. Endosymbiosis of an -proteobacterium taken up by an Asgard Archaea was a key step in eukaryogenesis [26].…”