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b) A. M. Gobe, R. Toro, X. Li, A. Ornelas, H. Fan, S. Eswaramoorthy, Y. Patskovsky, B. Hillerich, R. Seidel, A. Sali, B. K. Shoichet, S. C. Almo, S. Swaminathan, M. E. Tanner and F. M. Raushel, Biochemistry, 2013, 52, 6525–6536 CrossRef PubMed; a) C. J. Schwartz, O. Djaman, J. A. Imlay and P. J. Kiley, Proc. Natl. Acad. Sci., 2000, 97, 9009–9014 CrossRef CAS PubMed; Since eukaryotes obtained their biotin-dependent carboxylases from bacteria, we ignore them for the discussion concerning the cenancestor complement and we focus specifically on the respective ancestors of Archaea and Bacteria as intermediate steps between present-day species and the cenancestor. The components of biotin-dependent carboxylases have been duplicated, recombined and fused many times across evolution and, thus, many different evolutionary scenarios can be proposed. As it would be too long to discuss all of them, we will focus only on the one that we consider to be the most parsimonious (for examples of other scenarios see additional file 3). Although recent studies have revealed the importance of biotin-dependent carboxylases in Archaea, little is known about their origin and evolution [ 28, 29, 40]. These enzymes are much less abundant and diversified in Archaea than in the other two domains of life, but their study could be of major interest in understanding the emergence and ancient evolution of several central metabolic pathways in these organisms [ 58]. In Archaea, the BC domain is encoded by an independent subunit in both the PYC and the ACC-PCC complexes, instead of being a part of wider polypeptides. BC sequences are widespread among archaea and their phylogeny shows that major archaeal groups form monophyletic clades, which are more closely related among them than to any other taxon. This evidence supports the ancestral presence of the BC domain in Archaea and points to its vertical inheritance in this domain of life. Surprisingly, archaeal BC sequences do not cluster together with regard to the PYC and ACC-PCC functional groups, but rather following the accepted phylogeny of Archaea. This strongly supports the hypothesis for the presence of one unique promiscuous BC subunit in the last common archaeal ancestor that would have been recruited in both, PYC and ACC-PCC functions. In the other hand, the PCT phylogeny and its distribution in archaea also indicate that the PYC function may have existed in the archaeal common ancestor. Concerning the ACC-PCC function, the wide distribution of the CCT domain in archaea suggests that it could also be ancestral. Moreover, even though archaeal CCT sequences were not found to be monophyletic in our CCT phylogenies, the AU test could not reject the hypothesis of the archaeal monophyly, and thus the presence of a CCT subunit in the archaeal common ancestor can be hypothesized. As a result, one unique promiscuous BC subunit that collaborated with PCT and CCT subunits to catalyze their specific reactions may have existed in the last common archaeal ancestor. Interestingly, such a collaboration of a BC-encoding subunit with both the CCT and PCT systems has been suggested in Archaeoglobus fulgidus [ 59] although, to our knowledge, this has not yet been experimentally tested. Our analyses support to extend this possibility to the ancestor of Archaea. d) M. Fischer, A.-K. Schott, W. Römisch, A. Ramsperger, M. Augustin, A. Fidler, A. Bacher, G. Richter, R. Huber and W. Eisenreich, J. Mol. Biol., 2004, 343, 1267–1278 CrossRef PubMed;
b) S. O.-de Choudens, L. Loiseau, Y. Sanakis, F. Barras and M. Fontecave, FEBS Lett., 2005, 79, 3737–3743 CrossRef; A strong point of this scenario is its relative simplicity, relying on the general assumption of aggregative peptide domain architecture as a major force in protein evolution [ 63]. Noteworthy, this hypothesis assumes the independent emergence of the PT (ancient PYC) domain and the BT (bacterial XCC) domain. Thus, a convergent evolution has to be invoked to explain BT and PT structural resemblances. Despite that little is known concerning the characteristics and conservation of the BT/PT domains, their shared structure consisting of a conserved helix and several β-strands seems simple enough to hypothesize that it could have emerged twice independently and their conserved position between the BC and the BCCP domains could be the result of structural constraints related to their common subunit-interaction roles. S. Y. Gerdes, M. D. Scholle, M. D'Souza, A. Bernal, M. V. Baev, M. Farrell, O. V. Kurnasov, M. D. Daugherty, F. Mseeh, B. M. Polanuyer, J. W. Campbell, S. Anantha, K. Y. Shatalin, S. A. K. Chowdhury, M. Y. Fonstein and A. L. Osterman, J. Bacteriol., 2002, 184, 4555–4572 CrossRef CAS PubMed. Full size image Phylogenetic analysis of the CT domains: The CoA-related carboxyl transferase (CCT)Chapman-Smith A, Cronan JE: In vivo enzymatic protein biotinylation. Biomol Engineering. 1999, 16: 119-125. 10.1016/S1050-3862(99)00046-7.
D. M. Howell, M. Graupner, H. Xu and R. H. White, J. Bacteriol., 2000, 182, 5013–5016 CrossRef CAS PubMed. Rodionov DA, Mironov AA, Gelfand MS: Conservation of the biotin regulon and the BirA regulatory signal in Eubacteria and Archaea. Genome Res. 2002, 12: 1507-1516. 10.1101/gr.314502. Urea carboxylases (UCA; E.C. 6.3.4.6) fix a carboxyl group in urea to form allophanate, an intermediate product of a two-steps process of urea degradation. Allophanate is subsequently hydrolyzed by the allophanate hydrolase to ammonia and CO 2. While in Saccharomyces cerevisiae the allophanate hydrolase and the urea carboxylase are fused within the same polypeptide [ 43], in the alpha-proteobacterium Oleomonas sagaranensis and green algae these two functions are carried out by two independent enzymes homologous to the unique S. cerevisiae peptide [ 44]. The O. sagaranensis urea carboxylase is a polypeptide by itself containing a BC domain in its N-terminal end, a BCCP domain in its C-terminus and a predicted central CT domain non-homologous to the previously cited CTs. b) A. Bacher, S. Eberhardt, M. Fischer, K. Kis and G. Richter, Annu. Rev. Nutr., 2000, 20, 153–167 CrossRef CAS PubMed; Finally, the BC phylogeny indicates that UCA genes were acquired recently and independently by fungi and green algae from bacteria. Whereas eukaryotes have maintained the same domain structure than their bacterial counterparts for PYC, MCC, PCC and bacterial-type ACC, the components of eukaryotic ACC and UCA have fused to generate large polypeptides. Biotin-dependent carboxylases in Archaeaa) P. C. Dorrestein, H. Zhai, F. W. McLafferty and T. P. Begley, Chem. Biol., 2004, 11, 1373–1381 CAS; e) J. C. Morales, L. Li, F. J. Fattah, Y. Dong, E. A. Bey, M. Patel, J. Gao and D. A. Boothman, Crit. Rev. Eukaryotic Gene Expression, 2014, 24, 15–28 CrossRef PubMed; a) A.-M. Sevcenco, M. W. H. Pinkse, E. Bol, G. C. Krijger, H. T. Wolterbeek, P. D. E. M. Verhaert and P.-L. Hagedoorn, Metallomics, 2009, 1, 395–402 CrossRef CAS PubMed; Recent systems chemistry approaches have argued that the basic metabolic networks of life, 106,107 such as the TCA cycle and especially its reverse counterpart, the rTCA cycle, but also others, existed long before the appearance of LUCA. 108–110 These networks arose in parallel with RNA, which receives special attention in the RNA-world theory because of its catalytic and self-replicating capabilities. 101 e) M. Fischer, W. Romisch, S. Schiffmann, M. Kelly, H. Oschkinat, S. Steinbacher, R. Huber, W. Eisenreich, G. Richter and A. Bacher, J. Biol. Chem., 2002, 277, 41410–41416 CrossRef CAS PubMed;
a) J. R. Allen, D. D. Clark, J. G. Krum and S. A. Ensign, Proc. Natl. Acad. Sci. U. S. A., 1999, 96, 8432–8437 CrossRef CAS PubMed; b) X.-Y. Zhi, J.-C. Yao, S.-K. Tang, Y. Huang, H.-W. Li and W.-J. Li, Genome Biol. Evol., 2014, 6, 149–160 CrossRef PubMed. a) C. Shen, L. Yang, S. Miller and J. Oró, Origins Life Evol. Biospheres, 1987, 17, 295–305 CrossRef CAS; a) W. Lubitz, H. Ogata, O. Rüdiger and E. Reijerse, Chem. Rev., 2014, 114, 4081–4148 CrossRef CAS PubMed;Rodriguez E, Banchio C, Diacovich L, Bibb MJ, Gramajo H: Role of an essential acyl coenzyme A carboxylase in the primary and secondary metabolism of Streptomyces coelicolor A3(2). Applied Environ Microbiol. 2001, 67: 4166-4176. 10.1128/AEM.67.9.4166-4176.2001. d) H. Sakuraba, T. Satomura, R. Kawakami, S. Yamamoto, Y. Kawarabayasi, H. Kikuchi and T. Ohshima, Extremophiles, 2002, 6, 275–281 CrossRef CAS PubMed; Coenzyme M ( 22). Coenzyme M is found in methanogenic archaea where it has a key role in methane formation. 82 The S-methyl derivative is generated from coenzyme M ( 22) in methyl transfer reactions catalyzed by proteins containing zinc. Coenzyme M is also involved in the bacterial metabolism ( e.g. in proteobacterium Xanthobacter autotrophicus) of alkenes and oxiranes. 83 Dunn MF, Encarnacion S, Araiza G, Vargas MC, Davalos A, Peralta H, Mora Y, Mora J: Pyruvate carboxylase from Rhizobium etli: mutant characterization, nucleotide sequence, and physiological role. J Bacteriol. 1996, 178: 5960-5970. As previously mentioned, the BCCP domain is characteristic of all the biotin enzyme family, including the decarboxylases and transcarboxylases, whereas the BC domain is limited to the carboxylases. The CT domain gives its substrate specificity to each biotin-dependent carboxylase. Although all biotin-dependent carboxylases bear these three types of protein domains, their arrangement is unequal among different carboxylases and from one domain of life to another. This arrangement will be briefly summarized below (Figure 2B).
Bower S, Perkins J, Yocum RR, Serror P, Sorokin A, Rahaim P, Howitt CL, Prasad N, Ehrlich SD, Pero J: Cloning and characterization of the Bacillus subtilis birA gene encoding a repressor of the biotin operon. J Bacteriol. 1995, 177: 2572-2575. a) G. Gutzke, B. Fischer, R. R. Mendel and G. Schwarz, J. Chem. Biol., 2001, 276, 36268–36274 CrossRef CAS PubMed; Finally, although CCT homologues could be detected in a wide diversity of archaeal genomes, we did not retrieve the monophyly of these archaeal sequences in the CCT phylogenies. The statistical support for the separation into several archaeal subgroups was weak, so we tested the possibility that they actually form a monophyletic assemblage by using an unbiased AU test to compare the tree shown in Figure 5 with a tree in which we forced the monophyly of the archaeal sequences (see Methods). The latter could not be rejected by the AU test ( P = 0.12), opening the possibility that the archaeal sequences may be monophyletic and that the topology observed could be affected by a phylogenetic reconstruction artifact. Phylogenetic analysis of the CT domains: The pyruvate carboxylase carboxyl transferase (PCT) D. Harris, D. Lukoyanov, S. Shaw, P. D. Compton, M. Tokmina-Lukaszewska, B. Bothner, N. L. Kelleher, D. R. Dean, B. M. Hoffman and L. C. Seefeldt, Biochemistry, 2018, 57(5), 701–710 CrossRef CAS PubMed. An alternative origin of archaeal biotin carboxylases through ancient HGTs from bacteria cannot be completely excluded. However, except for some particular cases limited to some specific organisms, the distribution and the phylogenetic trees of the BC and the PCT domains are congruent with the expected phylogeny of Archaea. As a result, the hypothetical HGT events responsible for the presence of the BC and PCT domains in Archaea should have been ancient enough to predate the last common archaeal ancestor, and thus HGT cannot be favored over the simple vertical inheritance from the cenancestor. Concerning the CCT domain, some groups, as for example the Halobacteriales, may have inherited their sequences by HGT from bacterial donors, but our results do not provide enough support neither to the monophyly of all archaeal CCTs nor to the putative HGT-mediated origin of these sequences, so this issue remains open.Targeting sequences seem to be absent from eukaryotic PYC and ACC. Both BC- and PCT-domain phylogenies strongly support the branching of eukaryotic PYC sequences among their bacterial homologues, what indicates a bacterial origin even though the vector of this HGT cannot be specified. Surprisingly, concerning the eukaryotic ACCs, the phylogenetic reconstructions are at odds with protein domain comparison. On the one hand, eukaryotic ACCs branch among bacterial ACC sequences in preliminary CCT and accurate BC phylogenies (additional file 1 and Figure 3, respectively), suggesting that bacterial donors are at the origin to these sequences. However, eukaryotic ACC sequences form extremely divergent groups in both BC and CTT phylogenies, probably as a consequence of rapid evolution subsequent to the fusion of these domains to generate the eukaryotic ACC polypeptide. Thus, reconstruction artifacts are likely and little confidence can be given to the position of eukaryotic sequences in these phylogenies. On the other hand, protein domain composition of eukaryotic ACC is very different from those of PYCs and bacterial ACCs, but shares strong similarity with that of XCC (Figure 2). Huang et al. proposed that the most likely way to explain the unique domain composition of eukaryotic ACC is a fusion event between the α- and β-subunits of XCC on both sides of a central linker [ 27]. The elucidation of the function of the BT/PT domain of eukaryotic ACCs will be necessary to decide between the XCC and the bacterial ACC origin for the eukaryotic ACC polypeptides. b) D. C. Johnson, D. R. Dean, A. D. Smith and M. K. Johnson, Annu. Rev. Biochem., 2005, 74, 247–281 CrossRef CAS PubMed.
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