Abstract
Reconstructing the genetic traits of the Last Common Ancestor (LCA) and the Tree of Life (TOL) are two examples of the reaches of contemporary molecular phylogenetics. Nevertheless, the whole enterprise has led to paradoxical results. The presence of Lateral Gene Transfer poses epistemic and empirical challenges to meet these goals; the discussion around this subject has been enriched by arguments from philosophers and historians of science. At the same time, a few but influential research groups have aimed to reconstruct the LCA with rich-in-detail hypotheses and high-resolution gene catalogs and metabolic traits. We argue that LGT poses insurmountable challenges for detailed and rich in details reconstructions and propose, instead, a middle-ground position with the reconstruction of a slim LCA based on traits under strong pressures of Negative Natural Selection, and for the need of consilience with evidence from organismal biology and geochemistry. We defend a cautionary perspective that goes beyond the statistical analysis of gene similarities and assumes the broader consequences of evolving empirical data and epistemic pluralism in the reconstruction of early life.
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Notes
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Eric Bapteste and John Dupré (2013) have called attention to the standard model or entities ontology and have argued in favor of a processual microbial ontology. Although their arguments are relevant for our proposal and for our emphasis on cellular processes, we have restricted ourselves to a tangential reference to their ideas.
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On the question of pluralism, also, “[a]universal Tree of Life (TOL) has long been a goal of molecular phylogeneticists, but reticulation at the level of genes and possibly at the levels of cells and species renders any simple interpretation of such a TOL, especially as applied to prokaryotes, problematic.” (Doolittle and Brunet 2016, p. 1).
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A progenote is “a hypothetical biological entity in which phenotype and genotype had an imprecise, rudimentary linkage relationship” (Woese and Fox 1977).
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By locating 355 protein families, Weiss et al. inferred a set of traits, including that the LCA (which equivocally for the authors is the same as the progenote) was anaerobic, CO2 fixing, H2 dependent with a Wood–Ljungdahl pathway, N2-fixing and thermophilic, among many other biochemical details. What drew the most pointed critique, however, was the speculation that this organism consisted of a cell-sized compartment bound by a mineral membrane, a hypothesis that revealed the lack of familiarity with current advances in the biochemistry of lipids and on the geochemistry of hydrothermal vents (the supposed environment of this organism). This membrane had an “underlying lipid bilayer added to provide a permeability barrier to ions such as Na+ and H+”. But, as Gogarten and Deamer point out, an obvious question was the source of the lipid forming the membrane, and the process by which it would adhere to the mineral surface.
To this, they added a critique of the supposed ATP-ase and sodium–proton exchange mechanism embedded in the bilayer, finally concluding that “these biochemical systems and catalysts are characteristic of an advanced form of life having ribosomes, translation, genes and a genetic code, far beyond what most would imagine as the first form of life” (Gogarten and Deamer 2016).
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The complete methodological critique goes like this: “Weiss et al. propose a computational scheme that provides a shortcut to identify genes that may have been present in LUCA. This approach is subject to two types of error: False positives. The stated criterion for inclusion in the LUCA gene set is that the gene needs to be present in two archaeal and two bacterial groups. From the presented tables, it is clear that orders are considered as distinct groups. The criterion identifies a gene as present in LUCA if a single transdomain transfer occurred before the two ‘groups’ (that is, orders) in the receiving domain split, or if the transferred gene was subsequently transferred between the two groups. Given that gene transfer within domains occurs more frequently than transfer between domains, a large number of false positives are expected under the implemented scheme. False negatives, which are likely to be an even bigger problem. The authors correctly assume that gene transfer between the domains has occurred. Consequently, many genes that were present in LUCA will not be inferred as present. ATP synthases and aminoacyl-transfer RNA (tRNA) synthetases illustrate this point, because only one out of at least five ATP-synthase subunits was part of the inferred LUCA set, and only eight aminoacyl-tRNA synthetases, whereas LUCA appears to have used the full complement of today’s genetically encoded amino acids, and had a functional ATPase/ATP synthase. The consequence of these errors is that the inferred LUCA gene set is strongly biased toward genes that have a limited distribution and utility in today’s organisms'' (Gogarten and Deamer 2016, p. 1).
References
Bapteste E, Dupré J (2013) Towards a processual microbial ontology. Biol Philos 28:379–404. https://doi.org/10.1007/s10539-012-9350-2
Bapteste E, O’Malley MA, Beiko R et al (2009) Prokaryotic evolution and the tree of life are two different things. Biol Direct 4:34. https://doi.org/10.1186/1745-6150-4-34
Becerra A, Islas S, Leguina JI et al (1997) Polyphyletic gene losses can bias backtrack characterizations of the cenancestor. J Mol Evol 45:115–117
Becerra A, Delaye L, Islas S et al (2007) The very early stages of biological evolution and the nature of the last common ancestor of the three major cell domains. Annu Rev Ecol Evol Syst 38:361–379
Becerra A, Rivas M, García-Ferris C et al (2014) A phylogenetic approach to the early evolution of autotrophy: the case of the reverse TCA and the reductive acetyl-CoA pathways. Int Microbiol. https://doi.org/10.2436/20.1501.01.211
Cantine MD, Fournier GP (2018) Environmental adaptation from the origin of life to the last universal common ancestor. Orig Life Evol Biosph. https://doi.org/10.1007/s11084-017-9542-5
Callaway E (2020) ‘It will change everything’: DeepMind’s AI makes gigantic leap in solving protein structures. Nature 588(7837):203–204. https://doi.org/10.1038/d41586-020-03348-4
Cohen O, Gophna U, Pupko T (2011) The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol Biol Evol 28:1481–1489
Cortez D, Delaye L, Lazcano A et al (2009) Composition-based methods to identify horizontal gene transfer. Methods in molecular biology, vol 532. Humana Press, Totowa
Delaye L, Becerra A, Lazcano A (2005) The last common ancestor: what’s in a name? Orig Life Evol Biosph 35(6):537–554
Doolittle WF (1999a) Phylogenetic classification and the universal tree. Science 284(5423):2124–2128
Doolittle WF (1999b) Lateral genomics. Trends Cell Biol 9:M5–M8
Doolittle WF (2000) Searching for the common ancestor. Res Microbiol 151:85–89
Doolittle WF (2009) The practice of classification and the theory of evolution, and what the demise of Charles Darwin’s tree of life hypothesis means for both of them. Philos Trans R Soc Lond Ser B Biol Sci 1527:2221–2228
Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life hypothesis. Proc Natl Acad Sci USA 104:2043–2049
Doolittle WF, Brunet T (2016) What is the tree of life? PLoS Genetic 12:e1005912. https://doi.org/10.1371/journal.pgen.1005912
Dupré J (2003) Human nature and the limits of science. Clarendon Press, Oxford. ISBN: 9780199248063
Fournier GP, Andam CP, Gogarten JP (2015) Ancient horizontal gene transfer and the last common ancestors. BMC Evol Biol 15:70. https://doi.org/10.1186/s12862-015-0350-0
Galtier N, Tourasse N, Gouy M (1999) A nonhyperthermophilic common ancestor to extant life forms. Science. https://doi.org/10.1126/science.283.5399.220
Gogarten JP, Deamer D (2016) Is LUCA a thermophilic progenote? Nat Microbiol 1:1–2
Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19(12):2226–2238
Goldman AD, Bernhard TM, Dolzhenko E et al (2013) LUCApedia: a database for the study of ancient life. Nucleic Acids Res. https://doi.org/10.1093/nar/gks1217
Groussin M, Boussau B, Charles S et al (2013) The molecular signal for the adaptation to cold temperature during early life on earth. Biol Lett. https://doi.org/10.1098/rsbl.2013.0608
Hagen JB (1999) Naturalists, molecular biologists, and the challenges of molecular evolution. J Hist Biol 32:321–341
Hagen JB (2003) The statistical frame of mind in systematic biology from quantitative zoology to biometry. J Hist Biol 36:353–384
Harris JK, Kelley ST, Spiegelman GB et al (2003) The genetic core of the universal ancestor. Genome Res 13:407–412
Hilario E, Gogarten JP (1993) Horizontal transfer of ATPase genes–the tree of life becomes a net of life. Biosystems 31(2–3):111–119. https://doi.org/10.1016/0303-2647(93)90038-e
Holmes FL (2004) Investigative pathways. Patterns and stages in the careers of experimental scientists. Yale University Press. ISBN: 9780300100754
Huang J, Gogarten JP (2006) Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends Genet 22(7):361–366
Hügler M, Sievert SM (2011) Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annu Rev Mar Sci 3:261–289. https://doi.org/10.1146/annurev-marine-120709-142712
Husnik F, McCutcheon JP (2018) Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol 16:67–79
Jácome R, Becerra A, Ponce de León S et al (2015) Structural analysis of monomeric RNA-dependent polymerases: evolutionary and therapeutic implications. PLoS ONE 10:e0139001
Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. https://doi.org/10.1038/nrg2386
Kim KM, Caetano-Anollés G (2011) The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol Biol 11:1–25
Kim KM, Caetano-Anollés G (2012) The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms. BMC Evol Biol. https://doi.org/10.1186/1471-2148-12-13
Kleiner M, Petersen JM, Dubilier N (2012) Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer. Curr Opin Microbiol. https://doi.org/10.1016/j.mib.2012.09.003
Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1(2):127–136
Kyrpides N, Overbeek R, Ouzounis C (1999) Universal protein families and the functional content of the last universal common ancestor. J Mol Evol 49:413–423
Loewe L (2008) Negative selection. Nat Educ 1(1):59
Martin W, Baross J, Kelley D et al (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol 6:805–814
McInerney JO, Cotton JA, Pisani D (2008) The prokaryotic tree of life: past, present and future? Trends Ecol Evol 23:276–281
Mirkin BG, Fenner TI, Galperin MY et al (2003) Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol Biol 3:2
Morgan G (1998) Emile Zuckerkandl, Linus Pauling, and the molecular evolutionary clock, 1959–1965. J Hist Biol 1:155–178
Muñoz-Velasco I, García-Ferris C, Hernandez-Morales R et al (2018) Methanogenesis on early stages of life: ancient but not primordial. Orig Life Evol Biosph. https://doi.org/10.1007/s11084-018-9570-9
Mushegian A, Koonin EV (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci 93:1026810273
O’Malley MA (2010) Ernst Mayr, the tree of life, and philosophy of biology. Biol Philos 25:529–552. https://doi.org/10.1007/s10539-010-9214-6
O’Malley MA (2013) Philosophy and the microbe: a balancing act. Biol Philos 28(2):153–159
O’Malley MA (2018) W. Ford Doolittle: evolutionary provocations and a pluralistic vision. Dreamers, Visionaries, and Revolutionaries in the Life Sciences. In: Harman O, Dietrich MR (eds) Dreamers, visionaries, and revolutionaries in the life sciences. University of Chicago Press, Chicago
O’Malley MA, Martin W, Dupré J (2010) The tree of life: introduction to an evolutionary debate. Biol Philos 25:441–453. https://doi.org/10.1007/s10539-010-9208-4
O’Malley MA, Leger MM, Wideman JG et al (2019) Concepts of the last eukaryotic common ancestor. Nat Ecol Evol 3(3):338–344
Ouzounis CA, Kunin V, Darzentas N et al (2006) A minimal estimate for the gene content of the last universal common ancestor–exobiology from a terrestrial perspective. Res Microbiol 157(1):57–68
Puigbò P, Wolf Y, Koonin EV (2013) Seeing the tree of life behind the phylogenetic forest. BMC Biol 11:46
Ranea J, Sillero A, Thornton J et al (2006) Protein superfamily evolution and the last universal common ancestor (LUCA). J Mol Evol 63:513–525
Rivas M, Becerra A, Lazcano A (2018) On the early evolution of catabolic pathways: a comparative genomics approach. I the cases of glucose, ribose, and the nucleobases catabolic routes. J Mol Evol 86:27–46
Russell R, Saqi M, Sayle R et al (1997) Recognition of analogous and homologous protein folds: analysis of sequence and structure conservation. J Mol Biol 269:423–439
Sapp J (2009) The new foundations of evolution: on the tree of life. Oxford University Press, Oxford
Sober E (1988) Reconstructing the past: parsimony, evolution and inference. MIT Press, Bradford
Sobolevsky Y, Trifonov E (2006) Protein modules conserved since LUCA. J Mol Evol 63(5):622–634
Sterner B (2017) Individuating population lineages: a new genealogical criterion. Biol Philos 32(5):683–703
Strasser B (2019) Collecting experiments: making big data biology. University of Chicago Press, Chicago
Suárez-Díaz E (2014) The long and winding road of molecular data in phylogenetic analysis. J Hist Biol 47:443–478
Suárez-Díaz E, Anaya-Muñoz V (2008) History, objectivity, and the construction of molecular phylogenies. Stud Hist Philos Biol Biomed Sci 39:451–468. https://doi.org/10.1016/j.shpsc.2008.09.002
Theobald DL (2010) A formal test of the theory of universal common ancestry. Nature. https://doi.org/10.1038/nature09014
Velasco J (2018) Universal common ancestry, LUCA, and the tree of life: three distinct hypotheses about the evolution of life. Biol Philos 33:31
Weiss M, Sousa F, Mrnjavac N et al (2016a) The physiology and habitat of the last universal common ancestor. Nat Microbiol 1:9
Weiss M, Neukirchen S, Roettger M et al (2016b) Reply to ‘Is LUCA a thermophilic progenote? Nat Microbiol 1:16230. https://doi.org/10.1038/nmicrobiol.2016.230
Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859
Woese C, Fox G (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci 74:5088–5090. https://doi.org/10.1073/pnas.74.11.5088
Woese (1987) Bacterial evolution. Microbiol Rev 51(2):21
Yang AS, Honig B (2000) An integrated approach to the analysis and modeling of protein sequences and structures. III. A comparative study of sequence conservation in protein structural families using multiple structural alignments. J Mol Biol. https://doi.org/10.1006/jmbi.2000.3975
Yang S, Doolittle RF, Bourne P (2005) Phylogeny determined by protein domain content. Proc Natl Acad Sci 102:373–378
Zhou Z, Liu Y, Li M, Gu JD (2018) Two or three domains: a new view of tree of life in the genomics era. Appl Microbiol Biotechnol 102:3049–3058. https://doi.org/10.1007/s00253-018-8831-x
Acknowledgements
A. Estrada thanks the Posgrado en Ciencias Biológicas at the Universidad Nacional Autónoma de México, as well as Consejo Nacional de Ciencia y Tecnología (CONACYT) for their support with fellowship No. 460604. I also thank Professor Daniel Piñero for his advice. We also acknowledge the invaluable help of Vivette García Deister and Luis Delaye for their insight on this paper.
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Scholarship No. 460604 to A.E. (CONACYT).
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Estrada, A., Suárez-Díaz, E. & Becerra, A. Reconstructing the Last Common Ancestor: Epistemological and Empirical Challenges. Acta Biotheor 70, 15 (2022). https://doi.org/10.1007/s10441-022-09439-1
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DOI: https://doi.org/10.1007/s10441-022-09439-1